THE INTESTINAL PARASITES AND DIET ANALYSIS
OF THE SOUTHERN SEA OTTER
A Thesis
Presented to
the Graduate Faculty
California State University, Hayward
In Partial Fulfillment
of the Requirements for the Degree
Master of Arts in Biology
by
Scott L. Hennessy
_July 1972
Acknowledgements
I would like to thank the California State Department
of Fish and Game for the opportunity to work on the sea
otter. I am greatly indebted to Doris Baron, the librarian
of the Moss Landing Marine Laboratories, for her aid in
obtaining the required literature. I would also like to
thank Drs. Mary Silver, James W. Nybakken, and G. Victor
Morejohn for critically reading the manuscript.
Table of Contents
Abstract . . . . . . . . . . . . • • . . . • • . • . . . . • . . . . . . . . • . . . . . . . . . . . ii
I. General problem ••••••••.,oooooeoooo•••••••••••ee••• 1
II. Literatu.re review e •••••••••• 0. G •••••••••••••••• 0. 0 1
III. Materials and methods ........•.........•..•.•..... 5
IV. Results and discussion
v.
A. Parasites of the southern sea otter.
1. Corynosoma macrosomurn . . . . • . • . • . . . . . . . . . . . 11
B.
2.
3.
4.
Falsifilicollis altmani ...•.........•....
Falsifilicollis kenti
Falsifilicollis major
5. Discussion of the parasites and their
possible effect on the sea otter ••••• 0 0 ••
Food items of the southern sea otter
Genera 1 discussion ................. o •••• ••• o •• 1!1 ••
17
24
30
31
35
38
Literature cited ···········0·················•eeGeGCIO 42
i
Abstract
The intestinal parasites of the southern sea otter
are identified and the number of parasites per otter
recorded. The female otters were observed to have a
significantly higher parasite load than the male otters.
Two acanthocephalan genera were observed: Corynosoma
and Falsifilicollis. Falsifilicollis has not been
recorded previously for the sea otter.
The contents of the alimentary canal were examined
revealing mainly crab hard parts. Three new food items,
Blepharipoda occidentalis, Cryptolithodes sitchensis,
and Crepidula .adunca were observed.
ii
Introduction
I. General problem.
The purpose of this study was twofold: a) to deter-
mine the numbers and species of parasites of the southern
sea otter (Enhydra lutris nereis); and b) to identify
. food items from the hardparts of invertebrates in the
stomach and intestines of this mammal. The present study
is the first endeavor to examine and identify the parasites
of the southern sea otter. It is also the first detailed
survey of the otter's diet by analysis of stomach and
intestinal content. The previous studies of food habits
of the southern sea otter have dealt with observations of
food items being eaten by the otter and of scats left on
the shore by an individual otter (Vandevere, 1969).
II. Literature review.
Barabash-Nikiforov (1935) recorded Porrocaecum
decipiens Krabbe as well as an unidentified cestode from
the northern sea otter, Enhydra lutris Linnaeus. Morozov
(1957) described the acanthocephalan Corynosoma enhydrae
' from otters in the U.S.S.R. (Commander Islands). Afanas'ev
2
(1941) described t~e trematode Microphallus_pirum Afanas'ev
from the sea otters of the Commander Islands. Barabash
Nikiforov (1947) noted the presence of the cestode
Dyplogonoporus grandi Schulz in the scat of two captive
otters at Murman, U.S.S.R. Rausch and Locker (1951)
examined three sea otters for parasites from Amchitka,
Aleutian Islands, and collected four species of trematodes
and one species of acanthocephalan. The trematodes were
Orthosplanchnus fraterculus Odhner, Phocitrema fusiforme
Goto and Ozaki, Pricetrema zalophi Price, Microphallus
enhydrae n. sp., and an acanthocephalan of the genus
Corynosoma. Rausch (1953) recorded Corynosoma strumosum
Rudophi in addition to an undescribed species of this
genus. He also recorded Pyramicocephalius phocarum
Fabricius. The Corynosoma sp. collected by Rausch (1953)
was described as Corynosoma villosurn by Van Cleave (1953a).
Neiland (1962) described Corynosoma macrosomum from the
Alaskan sea otter. This species of Corynosoma appears to
be identical to the Corynosoma sp. found by Van Cleave
(1953b). Cestodes collected from a sea otter off Amchitka
Island have been identified as Diplogonoporus tetrapterus
Rausch. The nasal mite Halarachne miroungae sensu lato
was observed in about 3 percent of 200 otters necropsied
by Kenyon (1965).
3
It can be noted that the above records of parasites
for the sea otter are from the northern otters, and no
literature can be found which makes reference to para
sitism in the southern sea otter. Recent literature
concerning parasitism in the sea otter is a compilation of
the above records and descriptions of parasites for the
northern sea otter by Dailey and Brownell (1972), shown
in Table 1. The most recent literature, Margolis and
Dailey (1972), also concerns E. lutris.
Fisher (1939) was the first to examine the diet and
feeding behavior of the southern sea otter. She reported
the red abalone (Haliotis refuscens) to be the main con
stituent of the otter's diet with crabs, sea urchins, and
seaweed also being eaten.
Limbaugh (1961) reported from Monterey that the sea
otter ate red abalone, the rock scallop (Hinnites multi
rugosus), the mussel (Mytilus californianus), the red sea
urchin (Strongylocentrotus fransciscanus), various species
of snails, and possibly the chiton (Cryptochiton stelleri).
Boolootian (1965) made a comprehensive six year study
Table 1. Parasites recorded for Enhydra lutris of the north Pacific. (From Dailey and Brownell, 1972).
Trematoda
Microphallus pirum Orthosplanchnus fratercus Pricetrema zalophi Phocitrema fusiforme
Nematoda
Porrocaecum decipiens
Acanthocephala
Corynosoma strumosum Corynosoma villosum Corvnosoma enhydri Corynosoma macrosomum Corynosoma sp.
Acarina
Halarachne miroungae
Cestoda
Diplogonoporus tetrapterus Pyramicocephalus phocarum
4
5
and reported that the sea urchins made up 65.4 percent of
the otters diet followed by Mytilus californianus (33.8
percent) and abalones (8.2 percent).
Ebert (1968) working in the southern range of the sea
otter at Pica Creek reported the otter diet to include, in
addition to the above mentioned items, the rock crab
(Cancer antennarius), the gaper clam (Tresus nutalli),
and the kelp (Macrocystis angustifolia). Abalone (63.4
percent of biomass) and crabs (25.9 percent) dominated
the otter diet.
Vandevere (1969) enlarged the list of the otter's
diet items (Table 2).
All of the southern sea otter diet studies noted
above dealt with field observations of feeding otters.
Vandevere's study was a combination of field observation
and scat analysis. The present study entailed a study of
the otters diet by inspection of the stomach and intestinal
contents of this animal.
III. Materials and method
The California State Department of Fish and Game
provided the Moss Landing Marine Laboratories with the
-~
6
Table 2. Food items eaten by Enhydra lutris nereis. (From Vandevere, 1969).
Mollusca
Red abalone, Haliotis rufescens Black abalone, Haliotis cracherodii Turban snail, Tegula montereyi Owl limpet, Lottia gigantea California mussel, Mytilus californianus Rock scallop, Hinnites multirugosus Gaper clam, Tresus nutalli Opalescent squid, Loligo opalescens
Crustacea
Kelp crab, Pugettia producta Rock crab, Cancer antennarius Furry crab, Hapalogaster cavicauda
Annelida
Feather duster, Eudistylia polymorpha
Echinodermata
Ochre star, Pisaster ochraceus Sunflower star, Pycnopodia helianthoides Bat star, Patiria miniata Purple urchin, Strongylocentrotus purpuratus Red urchin, Strongylocentrotus franciscanus
Chordata
Stalked tunicate, Styela montereyensis
Phaeophyta
Macrocystis pyrifera
This list includes only those food items identified to the species level.
7
thirty-two sea otters examined in this study. The sea
otters were recovered by Fish and Game personnel from the
central California coast between Monterey Bay and Morro
Bay. The causes of mortality of the sea otters were
determined by necropsy. Deaths occurred from natural and
artificial causes.
During the sea otter necropsy the entire alimentary
canal was removed for examination and separated from the
connective tissue. The canal was then placed in a large
dissecting tray and covered with running water. The
stomach and intestines were then opened, washed, and
carefully examined for parasites.
During the examination of the sea otter stomach and
intestines for parasites, any identifiable food particles
were collected and refrozen or placed in a four percent
formalin solution. The food particles were later examined
for feasibility of identification to species level. The
soft fleshy parts were usually not identifiable and there
fore this study was concerned only with the identification
of hard parts of the food items.
When a section of a crustacean appendage or carapace
or a mollusk shell was recognized it was then compared to
the corresponding part of an entire animal of known species.
·~
The identified piece was then placed in an alcoholic
preservation solution.
8
Parasites attached to the intestinal mucosa were
gently excised with forceps and dissecting needle and
placed in fresh water for washing. Parasites found
floating in the intestinal fluids were collected, washed,
and preserved in 70 percent ethanol.
The parasites were processed by a modification of
methods described by Olson and Pratt (1971), Van Cleave
( 19 53b), and 0 lson (personal conmmnica tion, 1971) . The
parasites were processed by the following method:
a. The parasites were removed from the preservation
fluid and stained in a solution of 70 percent ethanol
and Semichon's acetocarmine stain until specimens became
a light rose pink.
b. The specimens were dehydrated slowly through a
series of ethanol solutions to 100 percent ethanol.
c. The specimens were cleared by slow addition of
xylene to a small amount of the 100 percent ethanol
solution containing the specimens.
d. Uncatalyzed Ward's Bio-Plastic synthetic resin
was added to the clearing solution until nearly 100
percent mounting medium was attained.
e. The resin saturated specimens were mounted in
thin sections of the catalyzed synthetic resin.
9
The acanthocephalans have a tendency to collapse
easily and the rare specimens collected have a spherical
proboscis that collapsed immediately upon removal from a
supporting medium. Van Cleave (1953b) suggested a tri
sodium phosphate solution for restoration of shrivelled
specimens. Specimens that collapsed were passed through
several dilutions of ethanol to distilled water and then
placed in a warm 0.5 percent solution of trisodium phos
phate until the worms became plump and pliable. The
specimens were then transferred to distilled water with
repeated changes to ensure complete removal of the deter
gent. The restored specimens were taken through the
dehydration series to 70 percent ethanol.
There is special terminology to describe the
acanthocephalans and their diagnostic features. The
terminology is discussed below and illustrated in Figure 1.
The hook covered proboscis is the anterior most section of
the worm and functions in attachment of the worm to the
~ntestinal wall of the host. The neck is the unspined
section directly posterior to the proboscis and the term
l N
p
Ft
Ht
Figure 1
Falsifilicollis altmani
Scale = 1.25 mm
P = Proboscis N :=::: Neck Pr = Praesoma Ft = Foretrunk Ht = Hindtrunk
10
·~
11
praesoma is used to describe the proboscis, neck, and the
spined section posterior to the neck. The fore trunk
is the anterior half of the trunk or main body and the
hind trunk is the posterior half.
IV. Results and discussion
A. Parasites of the southern sea otter.
1. Corynosoma macrosomurn Neiland, 1962.
The author of the present study has found
the southern sea otter to be infected with a species
of Corynosoma appearing to be identical to C.
macrosomum as described by Neiland (1962).
Observa.tions:
All measurements in the following sections
are given in millimeters with average valu~;; en
closed in parentheses.
Diagnosis:
Females 16.5 to 28.5 (23.0) mrn long by 2.0
to 3.5 (2.7) mrn maximum width. Males 9.0 to 18.5
(13.7) mrn long by 1.0 to 3.2 (2.0) mrn maximum width.
Maximum width occurring in both males and females
at the anterior region of the foretrunk. The
12
foretrunk region of the males proportionally more
inflated than that of the females. The short
neck, measuring 0.5 to 0.7 (0.6) mm long in
females and 0.4 to 0.6 (0.5) long in males, tapers
rapidly to the base of the proboscis. · Hind trunk
1.6 to 2.6 (2.1) mm maximum width in females, 1.0
to 2. 0 ( 1. 5) mm maximum width in males. The
posterior region of the trunk of both sexes slightly
inflated at maximum width tapering abruptly to the
caudal process which is approximately one-fifth
to one-third the diameter of the inflation
(Figure 2).
Trunk spination of females occurred ven
trally from base of neck to a point posterior to
maximum width of foretrunk and dorsal trunk spines
occurred from the neck base to a point at maximum
trunk diameter. Trunk spination in males similar
to females except ventral spination did not
extend as far to the posterior as in females. A
line drawn from the end point of ventral spination.
to the end point of dorsal spination in the female
would intersect a line drawn parallel to the body
axis at approximately a 45 degree angle. The same
A.
Figure 2. A.
B.
13
B.
Corynosorna rnacrosornurn. Male, note copulatory bursa at posterior end.
C. rnacrosornum. Female.
Scale = 4.0 rnrn.
14
ventral to dorsal line in the male would inter-
sect the axis at approximately a 70 degree angle.
Genital spines of both sexes nearly covered
the surface of the caudal process, and proceeded
to the anterior more so in the female.
* Proboscis cylindrical with maximum diameter . )
at the base, 1.5 to 2.0 (1.7) mm long by 0.3 to
0.5 (0.4) mm maximum width in females and 1.0 to
1.5 (1.2) mm long by 0.3 to 0.5 (0.4) mm maximum
width in males. Proboscis of both sexes provided
with 26 to 28 longitudinal rows of 3 to 4 unrooted
thorns and 17 to 18 hooks per row (Figure 3).
Hature embryos were 0.10 to 0.11 mm long by
0.035 to 0.040 mm wide. Testes of male ellipsoidal,
usually occurring in the lower half of the body.
There appeared to be six cement glands adjacent
to the testes as described for C. macrosomum of
the northern otter.
Van Cleave (1953a) recognized the presence
of an undescribed species of Corynosoma from a
sea otter taken off Simeonof Island off the south
coast of Alaska. He did not describe it at that
time since only one specimen was available.
Figure 3. A. Proboscis hook from C. macrosomum. Scale = 0.06 mm.
A.
a 1 = Length of hook. a2 = Thickness of hook. a3 = Length of root.
B. Egg of C. macrosomum. Scale= 0.10 mm.
15
Neiland (1962) had the opportunity to examine a
female otter from Hinchinbrook Island, Prince
William Sound. The otter was found to be in
fected with 60 worms which appeared identical to
the one specimen of Van Cleave. Neiland then
described this largest of all acanthocephalan
species parasitizing mammals as C. macrosomum.
Neiland considered the northern otter the
definitive host for C. macrosomum. There is no
published evidence of this parasite occurring in
its adult form in other mammalian hosts.
16
The C. macrosomum of the southern sea otter
appears to be identical to the C. macrosomum of the
northern otter except for a greater size variation.
The length of the C. macrosomum of the northern
otter ranged from 18.5 to 26.0 mm for the females
compared to the range of 16.5 to 28.0 mm for the
same parasite in the southern otter. The size
range for the male parasites of the northern
otter is 12.5 to 17.0 mm compared to the 9.0 to
18.5 mm range for the parasite of the southern otter.
Petrochenko (1956) noted that female
acanthocephalans often dominate numerically in the
17
infections, and in older infections males may be
absent. In the present study females did pre
dominate in most cases. The exact numerical
ratio could not be determined due to similarity
in appearance of the immature females to the
males of all ages; adult females are easily
distinguished from males by their greater size,
but the immature females are not easily separated
from the males without detailed examination,
which was not within the scope of this study.
The infection loads of C. macrosomum in
the southern sea otter ranged from an absence of
parasites to 511 worms per otter. The number
of parasites recorded per otter and statistical
analyses of the infection loads of C. macrosomum
are presented in Table 3. The females have sig
nificantly larger parasite loads than the males
(U-test, 95 percent level).
2. Falsifilicollis altmani Perry, 1942.
Figures 1 and 4.
Diagnosis:
Sexes were indistinguishable due to immaturity
18
Table 3. Parasite infection loads in the southern sea otter.
Otter I
Number
Fen··ale so-203 so-F5 so-121 so-113 so- 20lf so-201 so- 2LfiJ so-137 so-154 so-177 Total:
11
l'lean 104.82.
Male so- 210 so-110 so-216 so-202 so-19LI so-207 so-221 so- 224-so-118 so-13Li so-155 so-157 so-122 so-123 so-119 so-116 so-179 so-95 so-150 HLML-0-30 ~1LML- 0-31 Total:
21
Number c. c. macro- F.
SOil!UID ---25 40 30 88
200 92
511
117 50
1151
Variance =
33 16 10 57
3L>
1 100
27 75 25
2
10 11 35
21578.76.
of parasites per otter
kenti F. major f· a1tmani ---
3
3 0 0
Standard Deviation = 146.89.
6
6 6
6 6 6
Man-Whitney "U-test" Result: female meJian parasite 1oaJ different from male at the 95 percent level.
( - ) indicates no parasites found.
Mean= 20.76. Variance= 680.39. Standard Deviation= 26.08.
Figure 4.
Falsifilicollis altrnani. Seale = l. 25 rnrn.
19
20
of specimens. Worms 3.5 to 4.0 mm long by 1.0 mm
maximum width near center of trunk. Trunk 1.7
to 2.7 (2.2) mm long, cylindrical in shape with
trunk tapering slightly to the anterior to a point
of abrupt width decrease. At this point the
spined praesoma extends to the base of the
aspinous neck. The neck slender, slightly smaller
in diameter than the praesoma, and 0.7 to 1.0 mm
long and extending to the base of the proboscis.
Proboscis slightly inflated to spherical, covered
with 27 longitudinal rows containing 9 to 11
hooks per row. Proboscis 0.29 to 0.54 mm in
diameter. Length of proboscis hook near apex
0.042 mm and hook length near proboscis base 0.063 mm.
The proboscis hooks were measured as prescribed
by Petrochenko (1956) and the dimensions of a
hook are illustrated in Figure 3.
F. altmani from the surf scoter, as
described by Perry, differs from F. altmani from
the southern sea otter. The most obvious differ
ence is the smaller size of the specimens from
the otter (3.5 to ~.0 mm as compared to the length
of mature females, 10.5 to 14.0 mm) and mature males
(8.5 to 12.0 mm) described by Perry. The size
difference may be due to the sexual immaturity
21
of the parasites from the otter. Another size
difference which may be attributed· to immaturity
is the proportionally smaller proboscis of the
otter parasite (0.29 by 0.34 mm t9 0.54 by 0.50 mm
as compared to 0.62 by 0.50 mm to 0.68 by 0.95 mm).
The number of longitudinal proboscis hook
rows (27) of F. altmani in the otters is with-
in the range described for the species (25 to 30)
and the number of hooks per row (9 to 11) is also
within the range of the original description
(9 to 12). The length of the proboscis hooks of
the otter parasite are 0.042 mm near the proboscis
apex and 0.063 mm at the base of the proboscis.
These lengths are within the range of the proboscis
hooks from the original description (0.03 to 0.05'mm
and 0.03 to 0.06 mm respectively).
Falsifilicollis altmani was originally
described by Perry (1942) from surf seaters
(Melanitta perspicillata) and white-winged seaters
(M. deglandi) found dead and dying on Carmel beach,
Monterey County, California, in the winters of 1938
and 1940.
22
Perry examined in detail the alimentary tract
from the proventriculus posteriorly from one
surf scoter. Infection began posterior to the
gizzard and continued to the anus, although the
cecae were not infected. Worms became ·progres
sively smaller at the approach of the large
intestine, although there were a few small worms
scattered among the large ones throughout'the
small intestine. Infection was the heaviest
at the anterior end. According to Perry's cal
culations there were 1,482 worms in the 28,000
square millimeters of intestine. Perry also
stated that the heavy infection of the seaters
probably caused their deaths, or at least made
them very susceptible to secondary infection.
Falsifilicollis altmani was originally
designated as Filicollis altmani. Van Cleave
(1947) redescribed the anatomy of the genotype,
Filicollis anatis Schrank, and showed that the
anatomy of the praesoma of adult F. anatis
differed markedly from that of the other members
of the genus. He therefore removed the species
F. sphaerocephalus Bremser and F. altmani Perry
23
to the genus Polymorphus Luhe.
Webster (1948) felt that the genus Poly
morphus was too large and heterogeneous for easy
understanding and therefore proposed a subgenus,
Falsifilicollis, to include those forms pre
viously included in the genus Filicollis.
Yamaguti (1963) elevated Falsifilicollis
from subgeneric to generic status to include F.
altmani, Polymorphus kenti Van Cleave, .!:· major
Lundstrom, P. texensis Webster, and Parafili:.,
collis sphaerocephalus Bremser.
F. altmani has not been recorded in hosts
other than the seaters nor can the author locate
any further record of the worm since Perry's
original survey in 1938 and 1940.
The occurrence of F. altmani in the
southern sea otter is a new record. Only one of
the otters examined was infected with this species
and then only six specimens were found. The sea.
otter may have become infected with F. altmani
by ingesting an infected species of crustacean
which is usually eaten by the surf seater. The
seaters feed along sandy beaches presumably on
24
small fishes and invertebrates including the sand
crab, Emerita analoga (G. V. Morejohn, personal
communication, 1971). The life cycle of F. kenti
has been found to include E. analoga (Reish, 1950).
It is then possible that the closely related F.
altmani may also utilize a sand crab as its inter
mediate host. If this speculation is valid the
infection of the otter would require its eating
the sand crab or the normal intermediate host of
F. altmani.
Ken Wilson (personal communication, 1971),
an agent of the California Department of Fish and
Game, observed on March 2, 1971, an otter feeding
on what he described as E. analoga. The author
found no remains of E. analoga in the stomach
and intestinal contents of thirty-two otters but
did record a new food item, Blepharipoda occiden
talis from several otters. B. occidentalis is a
large sand crab and may be a host to juvenile
acanthocephalans.
3. Falsifilicollis kenti Van Cleave, 1947.
Figure 5.
Figure 5.
Falsifilicollis kenti. Scale = 4.0 mm.
25
26
Diagnosis:
Sexes not distinguished in this study' due to
immaturity and paucity of specimens. Worms 13.0
to 26.0 mm long by 1.0 to 2.0 mrn maximum width.
Body spindle-shaped with a constriction near the
middle which divides trunk into anterior and pos
terior sections. Proboscis spherical with a 1.44 mm
maximum diameter covered with 30 longitudinal rows
of 12 hooks per row. Hook length at proboscis
median 0.056 by 0.009 mm maximum width. Hooks
quite fine and difficult to count and measure.
Neck 2.2 to 3.0 mm long by 0.36 to 0.43 mm wide at
proboscis base, 0.29 to 0.43 mrn wide near middle,
and 0.18 to 0.36 mrn wide at junction of neck and
trunk. Body spination restricted to the forward
third of the anterior section above constriction.
The largest specimen (26.0 IIllll) with sparse body
spination, spines about 0.007 mrn long. The smallest
specimen (13.0 mm) with a heavier covering of large
spines about 0.021 mrn long. Embryos and cement
glands not observed.
A comparison of F. kenti as described by
Van Cleave and the F. kenti observed parasitizing
27
the sea otter reveals differences that may be
sufficient to consider the parasites observed in
the otter a new species or a subspecies. The
main differences are the greater number of
proboscis hook rows, the number of hooks per
row, and the larger size of the specimens from
the otter.
The F. kenti described by Van· Cleave (1947)
had 27 longitudinal rows of proboscis hooks with 10
to 11 hooks per row. The F. kenti observed in this
study have 30 rows of 12 hooks per row. The
hook sizes of the parasites observed by Van Cleave
varied little, being about 0.053 to 0.058 mm long
by 0.008 mm in diameter. The hooks of the otter
parasite are about 0.056 mm long by 0.009 mm in
diameter.
The maximum size of the immature specimens
observed by Van Cleave was 15.0 mm long; the maximum
size of the otter parasite was 26.0 mm long. The
proboscis diameters of the two sets of F. kenti
are about the same; the otter parasite has a probos
cis 1.44 mm in diameter as compared to the type
specimen with a proboscis 1. 5 mm in diameter. Van
28
Cleave noted the presence of minute spines on the
anterior trunk of immature males and the lack of
such spination on immature females. He could not
demonstrate that these spines actually projected
from the body wall. All specimens of F. kenti from
the otter displayed spination of the anterior trunk
and these spines were measurable and projected
from the body wall.
The F. kenti was described by Van Cleave (1947)
as Polymorphus kenti from the intestine of the gull
Larus argentatus collected at Kent Island, New
Brunswick, Canada.
Reish (1950) recorded F. kenti at Coos Bay,
Oregon, in the western gull (Larus occidentalis)
and the glaucous gull (Larus glaucescens). He then
examined the sand crab (Emerita analoga) at Coos Bay
and found juvenile acanthocephalans free in the mid
gut near the digestive gland. A number of these
juvenile forms were fed to laboratory rats which,
after 25 days, were found to be infected with imma
ture F. kenti. The length of these immature forms
was from 10 to 15 mm.
A survey was then made by Reish of 109 E.
analoga collected at Coos Bay, August 6, 1949.
Of this total 86 were mature animals and 23 were
immature. Of the adult E. analoga 82 were in
fected, a 95 percent incidence. The range of
infection was 1 to 17 with a median of 3 para
sites per crab. Of the 23 immature sand crabs,
12 were infected, of which only one contained
two parasites; each of the remainder contained
only one juvenile parasite. None of the
earlier stages of the life cycle of the parasite
was observed in the sand crab.
29
The habitat of the sand crab, the inter
mediate host, is in the intertidal sand. The
probable life cycle of F. kenti as described by
Reish is the following: eggs of the parasite are
passed in the feces of the gull; the filter-feeding
E. analoga could pick up the eggs and act as the
intermediate host; the gull would become infected
by eating infected E. analoga. However, Reish
found no remains of the sand crab
examined post mortem.
nine gulls
The occurrence of the six specimens of F.
kenti in the sea otter is a new record at the class
30
level and also a distribution record. The manner
in which the otter became infected with this
parasite may follow that speculated for F. altmani:
the otter may have eaten E. analoga and become
infected. This would be possible because host
specificity is low as indicated by infection of the
laboratory rats by F. kenti (Reish, 1950).
4. Falsifilicollis major Lundstrom, 1942.
Diagnosis:
Sexes were not distinguished due to immaturity
of specimens. Body spindle-shaped with a con
striction near the trunk middle. Worms 4.0 to
6.5 rnm long by 1.0 rnm wide. Proboscis ovate 0.54
in diameter by 0.72 rnm long. Proboscis covered
with 18 rows of 6 to 7 hooks per row. Hooks com
paratively large, 0.098 to 0.112 rnm long by 0.014 rnm
wide with a large root, those hooks occurring at
proboscis median largest. Neck 1.15 rnm long by
0.72 rnm maximum width at junction of neck and trunk,
tapers to base of proboscis where neck is 0.298 rnm
wide. The anterior section of trunk above con
striction covered densely with spines which are
0.028 mm long. Five specimens of the species
occurred in one otter (Figure 6).
A comparison of the F. major observed in
31
this survey with illustrations of the type specimens
observed by Lundstrom revealed a similarity of the
proboscis hook arrangement and trunk spination. The
original description recorded 16 to 20 longi
tudinal rows of 7 to 9 hooks per row, hooks 0.081
to 0.099 mm long and trunk spines 0.03 mm long.
The maximum size for the type specimens was
27.0 mm long for the female and 18.5 mm long for
the male. The smaller size of the otter parasite
may be due to the immaturity of the specimens.
F. major was described from the duck
Clangula clangula in Sweden. The appearance of
this acanthocephalan in the sea otter represents
a new distribution record and a new host record
at the class level.
5. Discussion of the parasites and their possible
effect on the southern sea otter.
F. kenti, F. altmani, and F. major are
basically similar in appearance, having a spindle-
Figure 6.
Falsifilicollis major. Scale = 1.0 mm.
32
33
shaped body with a central constriction, a long
slender neck, and a spheroid proboscis. The F.
altmani and F. major observed in this study have
proboscis diameters that overlap in size but they
are easily separated by the lower number of hook
rows, hooks per row, and larger hooks on the
proboscis of F. major. F. altmani and F. kenti
have similarities in their arrangement and number
of hooks on the proboscis but are easily separated
because of the much larger proboscis of F. kenti.
F. major can be distinguished from F. kenti and F.
altmani by its stout neck, which has a greater
degree of tapering from the body toward the proboscis.
In general, Rausch (1953) believed these
helminths probably affect the northern sea otter
little, although Kenyon (1969) found the northern
otter to be occasionally seriously infected with
trematodes and nematodes. In the present study the
southern sea otter was found to be free of parasites
other than the acanthocephalans and there is no
literature concerning the effect of these parasites
on sea otters.
Petrochenko (1956) considered in detail the
·~
34
pathological, anatomical and histological changes
in the intestines of ducks caused by the infection
of Filicollis anatis. He found that F. anatis
completely penetrated the intestine of the ducks
and concluded that most of the pathological effects
were caused by the penetration of the parasite into
the intestinal wall. This penetration caused
parts of the intestinal wall to become ulcerative
and necrotic with eventual perforation of the wall.
Innervation of the intestine was then disrupted
as well as its secretory and motor functions. In
addition, toxic compounds were found to be
secreted by the parasite at the height of infection.
Thus Petrochenko concluded that Filicollis has a
definite pathological effect on the duck, and
suggested a strong invasion of the parasite would
cause death to the host.
In this study Corynosoma was easily removed
from the intestinal mucosa where it penetrated
very slightly. There was no visible damage by
this parasite to the intestinal wall. However, it
is possible that this genus may have harmful
effects on the otter if, as observed by Petrochenko
for Filicollis, Corynos'oma secretes toxic com
pounds while in the heavy infestation loads
observed.
35
The harm caused by the three species of
Falsifilicollis to the otter populations would
probably be small, due to their rare occurrence.
These three species attach to the intestinal wall
with their bulbous proboscis deeply embedded in
the intestinal wall. Removal of the parasite must
be accomplished by dissection of the intestine.
Because of the manner of attachment these species
could cause damage to the intestine.
B. Food items of the southern sea otter.
The sea otter with its strong jaws and bunodont
molars is capable of crushing and grinding mollusks
and crustaceans to small particles. The most common
crustacean parts observed that were identifiable were
appendages and carapace sections. Various sections
of mollusk shells were observed and occasionally
opercula of marine snails were found.
Often an otter stomach would contain only one
species of food item, often in large quantities,
indicating that the otter was foraging specifically
for one species of food. Twice otter stomachs
were filled with the squid Loligo opalescens and
36
on two other occasions otter stomachs contained large
amounts of a previously unrecorded foqd item, the
mole crab, Blepharipoda occidentalis.
Usually a food item found in one otter was again
found in other otters, indicating that it may be a
common food item. But occasionally a species appeared
only once and often as a single specimen indicating
that it may be a rarely eaten item. Such is probably
the case with three other food items not previously
mentioned in the literature as food items of the
southern sea otter: Cryptolithodes sitchensis,
Crepidula adunca, and a stalked barnacle. Marine
algae also occurred occasionally in the stomach con
tents. The algae were found in such small quantities
that they may have been accidentally ingested while
the otter was feeding on some other item.
Table 4 lists the food items observed in this
study and the number of otters that contained each
item.
37
Table 4. Food items found in the stomach and intestines of Enhydra lutris nereis.
Mollusca
Mytilus californianus Mytilus edulis Clinocardium facanum Crepidula adunca Tegula brunnea Loligo opalescens
Echinodermata
Strongylocentrotus sp. Pycnopodia helianthoides
Arthropoda
Brachyura
Cancer antennarius Cancer magister Pugettia producta Pugettia richii
Anomura
Blepharipoda occidentalis Cryptolithodes sitchensis
Cirripedia '
A stalked barnacle
Thallophyta (Algae)
Phyllospadix sp. Cystosiera osmundacea Corallina sp.
Number of otters containing item
2 1 1 1 1 2
2 1
2 1
1
1 1 1
38
V. Discussion
The parasites observed in this study include one
species, Corynosoma macrosomum, that was observed in the
northern sea otter. The other three species belong to one
genus, Falsifilicollis, that does not usually occur in
mammals and has not been mentioned in the literature
as occurring in the sea otter.
The infection of the sea otter by the species of
Falsifilicollis may be accidental because this genus has
previously been recorded only in birds. The possibility
exists that, given sufficient time and continual reinfection
of the otters by this genus, Falsifilicollis may adapt
to the internal environment of the otter and become a
more common parasite of the otter by gaining the ability
to reach maturity within the otter intestine. If this
does occur the otter may be presented with the more
serious problem caused by the method of attachment of
Falsifilicollis. A continual survey in the future of the
sea otter parasites might detect such a change.
The intraspecific competition between the sea otters
"'with increased otter population and the competition between
man and the otter for the edible fauna of the near shore
region may cause the otter to extend its diet to include
items not usually eaten. This diet expansion may intro
duce the otter to new parasites which may or may not be
.able to adapt to the internal environment of the otter.
39
The source of the otter acanthocephalan infection is
the intermediate host which is a food item of the otter.
A survey of the food items of the otter disclosed that
crustaceans formed a major part of the otter diet and
probably one or several of these crab species are function
ing as the intermediate host. A study to complete the
life cycle of the acanthocephalans of the sea otter would
include a collection of the various crab species with
close examination of their haemocoels for encysted larval
acanthocephalans. Another approach might include labora
tory forced ingestion of viable acanthocephalan eggs by
the various crab species with subsequent haemocoel exami
nation for encysted stages. The viable acanthocephalan
eggs could be obtained from freshly dead otters with
acanthocephalan infections.
The larger number of female than male C. macrosomum
observed in the majority of cases in the present study
~nd also observed for other Acanthocephala by Petrochenko
(1956) may be related to the greater development of the
attachment system in the female worm (Petrochenko, 1956).
Sexual dimorphism in the morphological features of the
Acanthocephala may be linked with the physiological and
biological role of the female and male in the life of the
species. The female remains securely in the intestine
during the long periods in which it produces embryos,
40
while the biological role of the-male probably consists
only of fertilization of the females. Since fertilization
occurs only once in the Acanthocephala, the further
existence of the male is unimportant from the point of view
of the survival of the species. After fertilization of
the female, an enormous number of embryos develop over a
long period of time. A calculated maximum of 500,000 eggs
per twenty-four hour period were eliminated by the
Macracanthorhynchus hirudinaceous observed by Petrochenko
(1956).
The author can find no reason for the greater parasite
infection load of the female otter. A larger sample size
might show the difference to be due to the size of the
sample population observed in the present study.
There are other restrictions in the diet survey of
~this study arising from the cause of otter death and the
physical condition of the otter at death. A healthy otter
killed instantly would represent a better sample for
41
food analysis than would an otter wounded with limited
capacity for movement and food capture. The healthy
instantly killed otter would provide a more realistic
example of otter diet because of its more normal behavior
and feeding. Also a diseased otter might have similar
restrictions on its capacity for diving and feeding and
therefore would possibly not be feeding or feeding upon
anything obtainable. Many of the otter alimentary canals
examined contained little or no food residue. Because of
the wide range of factors, known and unknown, causing the
death of the otters presented in this study and because
of the relatively small sample size there must exist some
differences between what was observed in the otter diet
and what may occur in the natural population.
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Barabash-Nikiforov, I. I. 1935. Commander Islands. J. Mammal.
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44
Van Cleave, H. J. 1947. Analysis of the distinctions between the acanthocephalan genera Filicollis and Polymorphus with description of a new species of Polymorphus. Trans. Amer. Microscop. Soc. 66: 302-313.
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