J . Linn. SOC.
(Zool.), 45, no. 303, p. 17
With 1 tezt.$gure
Printed in Great Britian
On the small deep-sea shark Etmopterus spinax L., and its
cirripede parasite Anelasma squalicolu (Loven)
BY C. F. HICKLING,
Sc.D.
(Accepted for publication January, 1963)
Communicated by the ZooZogicaZ Secretary
INTRODUCTION
The material on which this paper is based was collected between the years 1927 and
1944, when the writer was in the Ministry of Agriculture and Fisheries. A large number
of voyages on commercial steam trawlers was made during those years, and those during
which very deep water was fished frequently gave samples of the small bathypelagic
shark Etmopterus spinax. A few deep-water hauls made by the research-vessel ' George
Bligh' also gave samples of this shark, which were especially useful because they were
made with a cod-end covered with shrimp-netting. I n the commercial trawler trips, the
Hake, Merluccius merluccius, was the species of fish sought, and the nets therefore had
the usual 2B-inch mesh in the cod-end. The samples taken by the commercial trawlers
therefore were much subject to mesh-selection, and the smaller fish were usually few or
absent in the samples. Much of the material was lost in the war years, but enough is left to
make a contribution to a knowledge of this curious case of parasitism, and further material
has become difficult to get.
All samples came from the hake grounds to the west of the British Isles, in depths
chiefly from 160 fathoms to 300 fathoms, and between the Iatitudes of 50" and 54" N.
Etmopterus is black in colour and has luminous organs in the skin. During the exploratory voyages of the 'Florence Brierley' off the north-west of Scotland this fish was taken
in depths from 120-140 to 360-380 fathoms (Hickling, 1928). It is undoubtedly bathypelagic in habit, as is shown not only by the nature of its food, which was recorded as the
Euphausian Meganyctipkznes and small Scopelid fishes with luminous organs (with one
record of a juvenile Gadus poutassou) ; but also by trials with vertical long-lines made by
the Research-Vessel 'George Bligh' in January, 1927. Lines with baited hooks were
suspended from buoys off the south-west of Ireland where the depth of the water was
greater than 300 fathoms. Etmopterus was caught on hooks fishing a t depths of 160,200,
222,228,257, and 258 fathoms below the surface, and so well in midwater.
THE LIFE HISTORY OF THE HOST
Etmopterus is one of the smallest of the sharks. Among some 4000 specimens handled
in the present series the largest had a total length of 52 cm., though most of the fish taken
in the commercial samples were between 35 and 42 cm.
It is ovo-viviparous, and in Table 1 the course of gestation is shown.
Females with inactive ovaries were most frequent from January to September, but
they may have been in either of two conditions. They may have been, especially in the
months from January t o June, pregnant females from which the young had been forced
by rough handling in the catch, especially on deck a t the end of the haul. During pregnancy the ovary returns to the inactive state in which only small eggs are visible in the
ovary. On the other hand, in August and September, they may have been genuinely
inactive between breeding seasons.
2
C. F. HICKLING,
Sc.D.
18
Table 1
Percentage of mature females with
Month
Jan. 1931
Feb. 1932
May 1930
June 1931
Aug. 1934
Sept. 1934
Sept. 1944
Nov. 1935
Inactive
ovaries
72.3
81.3
47.2
60.4
53.8
66.1
29.0
4.3
Ripe ovarian
eggs
6.6
1.4
27.1
2.1
41.6
32.0
56.4
75.5
Embryos
<3cm.
8.0
4-6
12.7
17.7
1-3
11.3
18.0
Embryos
> 3 cm.
10.1
11.9
13.0
19.8
Degenerate
ovaries
3-1
0.8
4.5
-
-
1.5
1.5
2.3
I n the table below are given the measurements of aborted embryos found lying in the
catch after a haul made in June, 1931.
Length, cm.
Frequency
3
-
4
3
5
4
6
1
9
8
1
7
4
10
8
-
11
4
12
6
13
3
Of the females which were in obvious breeding condition, those with ripe ovarian eggs,
which are of very large size, were most frequent from August to November, while the
highest proportion of females carrying advanced embryos occurred from January to June.
The data in Table 1 suggest that in Etmopterus the breeding period extends over several
months, that ovulation occurs chiefly during the autumn, and that the birth of the young
takes place mainly during the late winter and spring. There is no evidence that the period
of gestation extends over more than a year, as is the case with the much larger Spur-Dog,
Squcclus acanthias (Ford, 1921; Hickling, 1930).
Females with degenerating ovaries occurred irregularly, and their significance is not
known.
As to the fecundity of the female ;the largest number of ripe ovarian eggs found was
14, the largest number of eggs developing in the oviducts was 12, and the largest number
of advanced embryos was 6, each of 11 cm. length. The tendency was for fewer embryos
to be found per female, the more advanced the embryos. This probably means that, the
nearer the embryos are to birth, the more easily they are aborted by the rough handling of
capture. This seem8 to be confirmed by the measurements given above of abortedembryos.
The yolk-sac is almost completely absorbed a t a length of 11 cm., only a small buttonlike remnant showing. The largest embryos found measured 13 cm., and were completely
ready for birth.
The production of even 6 embryos, each of 11 cm., is a notable feat for a fish of only
40 cm. total length.
I n Table 2 are given the lengths of embryos found in the oviducts. Since all the embryos
are at the same stage of development and have the samelength in anygivenfemale,each
entry in the table is the length of one embryo as representative of the whole litter.
Table 2. Length-Frequency of Embryos measured
Month
<4
4
5
6
7
Length (cm.)
8
9
10
11
12
13
Jan. 1931
Feb. 1932
May 1930
June 1931
Aug. 1934
Sept. 1934
Sept. 1944
Nov. 1935
19
9
30
17
2
4
3
5
2
1
6
4
3
4
2
4
3
6
3
7
2
2
2
0
3
2
5
6 1
4
1
7
2
1
1
3
-
3
7
81
4
2
3
3
3
4
3
- 1
On the small deep-sea slzark and its Cirripede parasite
19
The largest embryos were 13 cm. in length, and were found from January to June; the
largest proportion of advanced embryos was found in June. From August t o November
no embryos were measured greater than 5 cm., and most were at a very early stage of
development. But the frequencies of the more advanced embryos may have been masked
by abortion, especially as this becomes more frequent in the more advanced embryos.
This may also explain why there is not a more regular progression in the lengths of the
embryos towards birth in Table 2.
THE RATE OF GROWTH
The only evidence as t o the rate of growth comes from measurements of a catch made
by the research-vessel ' George Bligh' in August, 1931, when using a cod-end covered with
shrimp-netting, and these are shown in Figure 1 as a length-frequency diagram.
30
20
1c
Fig. 1. Length-Frequency distribution of an unselected sample of Etmopterw, spinax L.
taken with a covered cod-end.
The smallest fish were 12 cm. in length, and this slight overlap with the measurements
of the embryos given in Table 2 confirms that birth occurs a t a length of 12-13 cm.
Figure 1shows a mode for males a t 14 cm., and one for females a t 15 cm. This group of
young fish must obviously have been born in the previous few weeks, and this confirms
that birth is most frequent in the months about May to July. There is a second mode a t
about 27 cm. in both sexes, and these may be second-year fish, the growth in the first year
of life being therefore about 14 cm. I n the fish caught by the commercial trawlers, in spite
of mesh-selection, there are indications of the presence of a group of young fish of a length
between 25 and 30 cm., in several samples.
Beyond this the fish tend to form a single group for each sex, and probably represent
all the older year-groups compressed together in length by a slowing-downof the growthrate with increasing age and the onset of maturity.
I n all the commercial samples the females reach a greater size than the males; most
males are between 35 and 38 cm. in length, whereas most females are between 38 and
C. F. HICKLING,
Sc.D.
20
44 cm. The deeper the water from which the samples were trawled, the larger the size of
the fish, a distribution well known in many other species of fish. The larger the fish, the
greater the proportion of females, so that samples from the deeper water are composed
almost entirely of females. This may be illustrated in the comparison below.
--
Length of females (cm.)
Ground
Bull
Farm
Depth
(fm.1
170-190
300
Range
23-44
3648
Mean
39
42
Percentage of males
21
7
An exception to this was found in the June sample from about 190 fathoms, where the
mean length of the females was 35 cm. and the percentage of the males 53. But this sample
was taken at a time when all the males were running with milt; and since the fish were
obviously breeding, an equality in the proportion of the sexes would be expected.
I n the youngest group of new-born fish shown in Figure 1, the ratio of males to females
was 46 :54, and in the second group 41 :59. The sexes are born in about equal numbers,
but as they grow older they become distributed, especially in relation to depth, so that
there is a preponderance of females in the deeper water.
MATURITY
Maturity in the males is shown by the enlargement of the testes and by the full development of the ‘ claspers’, which have been described by Jungersen (1899) and Leigh-Sharpe
(1920, 1922). I n the present series the largest normal immature males were 34 cm. in
length, the smallest mature males 30 cm. A t 33 cm. there were equal numbers of mature
and immature males. So maturity sets in a t a length of about 33 cm., and, by comparison
with Figure 1, in the third year of life.
But there is an interesting group of males, found especially in samples from the deeper
water, which have ‘claspers’ of the immature type and which have no gonads a t all.
I noted them as ‘infantile’ or ‘senescent’ males. Most were of lengths from 39 to 46 cm.,
and in fact all males longer than 41 cm. were ‘infantile’. But there were a few between
34 and 38 cm., thus overlapping with normal males. The ‘ claspers’ of these fish showed no
indication of having regressed from the normal mature state with the armament of spines
well described by the authors mentioned above. They are therefore probably males which
have failed to develop normally because of the atrophy of the testes; and their accumulation among the largest fish may be due to a faster growth rate or greater longevity. They
are ‘capons’, and their livers are very fat. None of them showed signs of having been
parasitized.
Maturity in the females is shown by the development of the ovaries and of the oviducts.
An adolescent stage can be distinguished in which the ovaries are enlarged while the
oviducts are still narrow. Within these definitions, the largest immature female was
40 cm., the smallest mature female 33 cm., while mature and immature females were in
equal numbers a t about 36 cm. Females in the adolescent stage ranged in length from
33 t o 39 cm. Maturity sets in a t a larger size in females than in males.
A few females had degenerate ovaries (Table 1).They had a range in length from 35 to
49 cm., and most were between 41 and 46 cm. These fish, like the ‘infantile’ males, had
very fat livers.
THE LIFE-HISTORY OF THE PARASITE
The anatomy of Anelaswm has been described by Johnstone and Frost (1926). It is a
functional hermaphrodite, and the egg-sacs or ovigerous lamellae are usually visible
between the thorax and mantle lobes. The eggs are at all stages of development; and while
On, the small deep-sea shark a i d its Cirripede parasite
21
in the present series no detailed observations were made on the breeding cycle, developing
eggs were found in the ovigerous lamellae in January, May, August, and September. So
it seems probable that the production of nauplii occurs the year round. The nauplius larva
is a typical Cirripede Nauplius, and has been described by Frost (1928).
Attachment of the parasite to the host is most frequently a t the base of one of the dorsal
fins, and usually the first dorsal. This may be illustrated in the list below, where the
frequency of attachment at various positions is shown.
I n front of, or beside the first dorsal in 61 fish
I n front of, or beside the second dorsal in 13 fish
Above pelvic fins in 4 fish
Above pectoral fin in 1 fish
Clearly, attachment a t positions other than the first dorsal is exceptional.
Etmopterus has a long and very sharp spine in front of each dorsal fin. Before birth, this
is covered by a sheath of skin. After birth, this sheath ruptures to expose the spine,
leaving a circular scar around the base of the spine. There can be no doubt that this scar
is the most favourable site for the attachment of the first parasite, and explains the high
proportion of attachments a t that point.
The parasite soon differentiates into a capitulum, which remains visible externally,
and a peduncle which penetrates into the muscles of the host and later comes to contain
the ovaries. Roots grow out from the peduncle into the muscles of the host; yet the
capitulum retains its mouthparts and biramous appendages. The tissues ofthe host adapt
themselves to the presence of the peduncle by forming round it a ‘ cavity of implantation’
which is not in any sense a sore, for the tissues remain clean and healthy.
The number of parasites present on any one host is shown below.
11 fish had one parasite each
70 fish had two parasites each
4 fish had three parasites each
1 fish had four parasites (but in two lots of two each)
It is unusual t o find only one parasite on a fish, and where they occur they are of a small
size. I n eight of these cases the parasite was measured from the tip of the capitulum to the
base of the peduncle, as dissected out of the host. These measurements were 8, 8, 12,
13,14, 16, 17, 17 mm.
Evidently, soon after the attachment of the first parasite it is joined by a second, and
exceptionally a third. The ‘cavity of implantation’ of the first parasite again forms a
favourable site for the attachment of fresh larvae. But the first infection need not be
confined to very young fish. For example, a fish of 39 cm. total length had two parasites
measuring 9 and 11 mm., thus probably recently established. The spine pocket of the fish
therefore continues to be a favourable site for the attachment of the larvae of the parasite.
Generally speaking, the parasites on any given fish tend to be alike in size; but there
are many cases where there may be a 10-nim. difference in size between the smallest and
largest parasite. This may be seen in the list below:
Lengthoflargest 15 16 18 19 20 21 22 23 24 25 26 27 29 30 32 33 34 35
Lengthofsmallest 9 6 6 10 9 13 13 12 17 18 15 23 21 18 18 20 26 25
No case was found where a very small and a very large parasite were found on the same
fish, and no very young parasites were found where the first parasite was more than
18 mm. long. But maturity, as indicated by the swelling of the peduncle with the development of the ovaries within it, sets in a t a length of about 16 mm. Johnstone and Frost
found that parasites less than 10 mm. long were always immature, while those over 20 mm.
generally had egg-sacsin the mantle cavity. SOthe above data suggest that the ‘cavity of
C. F. IIICI(LINGI,
Sc.D.
22
implantation’ ceases to be a favourable site for the attachment of further parasites soon
after the peduncle swells with the development of the ovaries.
All the parasites dissected out and measured had the following length-frequency
distribution in 5-mm. groups:
Length
Frequency
%frequency
1 4
2
1.1
5-9
12
7.0
10-14
33
19.3
15-19
38
22.2
20-24
40
23-4
25-29
26
15.2
30-34
19
11.1
35-39
1
0.6
The greatest number of parasites were between 15 and 24 mm. in length, and the frequency
decreases rapidly among the larger fish parasitized.
Table 3
Length of host
(cm.)
Number of fish
15-19
20-24
25-29
30-34
35-39
40-44
45-49
2
28
102
250
968
1031
125
Number
parasitized
Percentage
parasitized
-
-
10
12
44
21
2
9-8
4.7
4-5
2.0
1.6
In Table 3 is given the percentage infestation at each centimetre group of Etmopterus
by one or more Anelasma. The table shows that there was nearly a 10% infestationin
fish of 25-29 cm., but that the rate then decreased to only 2% or less at lengths greater
than 40 om. This might mean that the parasitized fish grow more slowly than the others,
or that the older fish get rid of their parasites, which would then have a life-history
shorter than that of their host. But no case was seen where a fish had obviously just lost
its parasites. It was generally found that the length of the parasites (or a t least the
largest of them where more than one is present) is in relation to the length of the host, so
the frequency of the larger parasites should decline with the decline in the frequency of
the larger hosts. But the differential decrease in the frequency of the parasite among the
larger fish, shown in Table 3, probably indicates that the parasite eventually kills the
host and perishes with it.
Taking all the samples together, there was a gross rate of parasitism of 4.8% in the
males, and 3.1% in the females. But no significance need be attached to this difference
between the sexes, because the female Etmopterus grows to a greater length than the male,
and the larger fish, as Table 3 shows, have a declining rate of parasitism. I n the same way,
the data show no seasonal variation in the rate of parasitism, for the apparent variations
observed are associated with length-variationsin the samples of the host fish.No seasonal
variation would in any case be expected where the parasite apparently breeds the year
round and has a Me-span of more than one year.
THE EFFECT O F THE PARASITE ON TEE HOST
The parasite retains its normal Cirripedetrophic organs, and Johnstone and Frost quote
cases where there may have been food particles in the gut. But there seems to be no doubt
that the parasite takes all its nourishment fiom the host through the system of rootlets
which grow out of the peduncle into the muscles. This would be a drain on the resources
of the host which might be shown in the weight of the liver, which is the main storage
organ.
I n Etmopterus, as in a number of other much larger deep-sea sharks such as Scymnorhinus, Centroscymnus, and Oxynotus, which were also not uncommon in the catches of
On the s m l l deep-sea shark and its Cirripede parasite
23
the trawlers in very deep water, the liver is a n organ of remarkable size. While it is undoubtedly the chief storage organ, the fat stored there is more than a metabolic reserve,
for i t is principally squalene, a low-density fat which plays an important part in the
buoyancy of the fish (Denton, 1961).
Bulk weighings were made in three batches of Etmopterus in April, 1927, and gave the
following results :
Males
Females
Females
Mean length
(cm.)
36.0
35.5
40.5
Mean weight of liver
(g.)
36
35
55
Mean weight of fish
(69)
166
156
205
These weighings show that the weight of the liver equals 21,22, and 27% of the weight of
the gutted fish. I n Squalus acanthiaa i t is 9 to 13% (Hickling, 1930).
Table 4
Mean weights of the liver (g.)
A
r
Length
(om.)
Females
Males
38
39
41
42
43
44
34
37
38
With inactive With ovarian
ovaries
eggs
34.1
37.9
44.5
44.8
54.0
52.1
37.6
35.0
45.2
-
56.9
65.5
7
Pregnant
Parasitized
31.4
38.3
39.9
36.0
53.8
34.5
40.0
42.0
40.0
50.0
45.0
-
Normal mature
Parasitized
21.7
29.3
28.2
25.0
32.0
22.0
I n Table 4 are given the lengths and the weights of the livers of normal fish, for comparison with those of parasitized fish. The table shows that the smaller parasitized fish
have livers as full as those of normal fish, but that the larger parasitized fish have much
thinner livers, suggesting that the presence of the parasite becomes a serious drain on
the resources of the host.
This drain would be quantitative; but there are signs that there may also be a qualitative
drain also. While the present series confirm Johnstone and Frost in finding no sign of
castration of the host such as is caused in crabs by Sacculinu, the presence of the parasite
results in a marked reduction in reproductive capacity. No case was found in the present
series where a parasitized female Etmopterus was pregnant, and in only one case was there
even some enlargement of the eggs in the ovary. The four-fold table below shows that,
had the parasite had no effect on the host, a considerable proportion of the parasitized
females should have been in a breeding condition.
Non-parasitized
Parasitized
Total
Mature Female Etmopterus
With inactive
With active ovaries
ovaries
or pregnant
443
61 1
41
1
484
612
Total
1054
42
1096
The value o f ~ is
2 50.7, so it is very unlikely that the absence of breeding activity among
mature parasitized females is due to chance.
C. F. HICKLING,
Sc.D.
24
Among male parasitized Etmopterus, the testis in most cases showed a marked reduction
in size, being reduced to threads in many specimens. It proved difficult in the field t o give
a numerical value t o the volume of the testis, and they were simply recorded as ‘reduced’,
‘vestigial’, or ‘reduced to threads’.
I n the four-fold table below, i t can be seen that there can be some reduction in the size
of the testis in normal fish, while some of the parasitized fish showed a testis of apparently
normal size.
Non-parasitized
Parasitized
Total
Mature male Etmopterus
With normal
With reduced
testis
testis
422
2
4
24
426
26
Total
424
28
452
Again, x2 is calculated at 353, a value which makes it very unlikely that the observed
reduction in the size of the testis in parasitized fish is due to chance.
Yet the larger of the parasitized testes, a t all events, were producing spermatozoa, as
shown in stained transverse sections, and no case was seen where there was any tendency
for the male to acquire female characteristics and vice versa. The ‘infantile’ males have
already been dealt with; they have no testis a t all, and their condition appears to have no
connexion with parasitism.
SUMMARY
1 . Etnwpterus s p h x L. is a small bathypelagic shark which did not exceed 52 cm. in
length among 4000 specimens handled in the present series. The female grows to a larger
size than the male, and the fish is ovo-viviparous; ovulation occurs chiefly in the autumn,
and parturition in late winter and early spring, the period of gestation being less than a
year. The young are born a t a length of 12-13 cm.
2. The Cirripede parasite of this fish, Anelasma sqwcliwla (LovBn)appears to breed the
year round. It probably establishes itself first in the spine-pocket, especially that of the
spine in front of the first dorsal fin; and the peduncle of the parasite, penetrating deeply
into the muscles of the host, forms a ‘cavity of implantation’ convenient for the attachment of a second and exceptionally third parasite.
3. The parasite does not exhaust the resources of the host a t first, though i t appears t o
do so among the larger fish. The fertility of the host is significantly affected, though there
is no sign of parasitic castration’.
REFERENCES
DENTON,
E. J., 1962. Some recently discovemd buoyancy mechanisms in marine animals. Proc. Roy.
SOC.,A, 265: 366-70.
FORD,
E., 1921. A contributionto our knowledge of the life-historiesof the dogfish landed at Plymouth.
J . Mar. Biol. Assn. N.S., 12 : 468-505.
FROST,W. E., 1928. The nauplius larva of Anelasma squalicoh (LovBn). J . Mar. Biol. Assn., 15:
125-2 8.
HICKLINQ,
C. F., 1928. The exploratory voyages of the ‘Florence Brierley ’. Notes on the fish recorded.
Ann. Mag. Nut. Hist., (10) 2: 196-209.
HICKLINQ,
C. F., 1930. A contribution towards the life-history of the spur-dog. J. Mar. Biol. Assn.,
16: 529-76.
JOHNSTONE,
J. & FROST,
W. E., 1927. The cirripede fish parasite Anelasma squalicoh (Lovdn); its
general morphology. 35th Lancashire Sea-Fisheries Laboratoq Report for 1926 :29-91.
JUNGERSEN,
H. F. E., 1899. On the appendices genitales (claspers)in the Greenland shark,Somniosus
microeephalus (BI. Schn.), and other selachians. Danish Ingolf-Exped., 2 (2): 1-88.
LEIGH-SHARPE,
W. H., 1920. The comparative morphology of the secondary sexual characters of
elasmobranch fishes. J. Morph., 34: 245-65.
LEIGH-SRARPE,
W. H., 1922. The claspers, clasper siphons, and clasper glands. J . Morph., 36: 221-34.