OOGENESIS AND GONAD DEVELOPMENT IN THE COLD WATER
LOLIGINID SQUID LOLIGO GAHI (CEPHALOPODA: MYOPSIDA)
ON THE FALKLAND SHELF
V.V. LAPTIKHOVSKY AND A.I. ARKHIPKIN*
Fisheries Department, Falkland Islands Government, P.O. Box 598, Stanley, Falkland Islands Email: [email protected]
(Received 10 December 2000; accepted 23 April 2001)
ABSTRACT
Oogenesis and gonad development were studied on histological sections of the ovaries of 12 females
(98–165 mm mantle length, ML, I–V maturity stages) of the abundant Patagonian squid Loligo gahi
sampled from the south-eastern part of the Falkland shelf. Additionally, reproductive systems of 136
females (80–300 mm ML, I–V maturity stages) were analysed microscopically to find atretic oocytes
within the gonad. It was shown that the process of the oocyte development in the gonad and number of
oogenetic stages in L. gahi are similar to those described before in a number of temperate loliginid
species. However, development of both yolkless and vitellogenic oocytes in L. gahi is shifted to the
earlier stages of the reproductive system maturation, giving probably more time for the yolk accumulation at low metabolic rates in cold water. Oocyte resorption was observed in the majority of mature
females, but the proportion of atretic oocytes is always very low (about 1% of the total number of
oocytes) showing a relative unimportance of this process in the L. gahi oogenesis.
INTRODUCTION
The Patagonian squid Loligo gahi Orbigny, 1835
inhabits shelf and continental slope waters off the
southern part of South America (Roper, Sweeney &
Nauen, 1984). This relatively small loliginid squid is
the most abundant around the Falkland Islands, where
it supports one of the largest loliginid fisheries in the
world with the average annual catch being around
60,000 tonnes (FIG, 2000). During the last decade,
different aspects of the L. gahi biology including population structure, growth and maturation were intensively studied (Hatfield & Des Clers, 1998). It was
revealed that this squid is the most cold water species
among loliginids, developing, growing and maturing in
cold waters of subantarctic origin (Hatfield & Murray,
1999). L. gahi have a number of adaptations for cold
water spawning and egg development, including a high
proportion of yolk oocytes in the ovary, numerous
spawnings, short egg capsules containing a small
number of eggs, large eggs (2.2–2.5 mm diameter) and
hatchlings (3.1–3.4 mm mantle length), and shift of the
main spawning peak to spring (Arkhipkin, Laptikhovsky & Middleton, 2000; Laptikhovsky, Arkhipkin, Middleton & Butcher, in press). Females were
found to attach their egg clusters to the kelp stipes
nearshore (Arkhipkin et al., 2000). First estimations of
the potential fecundity did not exceed 2,000 eggs, how*Corresponding author.
J. Moll. Stud. (2001), 67, 475–482
ever, small oocytes were not counted (Hatfield, 1992).
Recent studies gave the higher potential fecundity of
1,800–35,200 oocytes of all size groups (Laptikhovsky
et al., in press).
The oogenesis of cephalopods, characterized by the
deep penetration of follicular folds into the oocyte and
role of the follicular syncytium in yolk production has
been studied in many inshore, temperate, loliginid
squid, such as Loligo vulgaris (Yung, 1930; Konopacki,
1933), Alloteuthis subulata (Bottke, 1974), Loligo pealei
(Selman & Arnold, 1977), Loligo opalescens (Knipe &
Beeman, 1978) and Loligo forbesi (Lum-Kong, 1993).
The correspondence between stages of oocyte development, phase of gonad development, and the maturity
stage of the squid reproductive system was shown,
however, only for L. pealei (Burukovsky & Vovk,
1974), L. vulgaris reynaudii (Sauer & Lipinski, 1990)
and L. bleekeri (Baeg et al., 1993). Neither oogenesis
nor gonad development has been studied in detail for
L. gahi. A preliminary histological examination of the
ovaries of L. gahi and a comparison of observed percentage of eggs with macroscopic maturity stages (Lipinski, 1979) was done by Comiskey (1996, cited in
Hatfield & Murray, 1999). Unfortunately, this study
has not been published. Moreover, it was done using
the simplified scale of oocyte stages of Sauer & Lipinski
(1990), where protoplasmic oocytes were evidently
confused with oogonia, that has recently been corrected by Melo and Sauer (1999). Thus, the main aim of the
© The Malacological Society of London 2001
V.V. LAPTIKHOVSKY & A.I. ARKHIPKIN
present study was to reveal whether L. gahi developed
specific adaptations for oogenesis and gonad development in cold water as it did for other reproductive
parameters, and to compare them with those of wellstudied temperate loliginids. Recently, the phenomenon of oocyte resorption was shown for L. vulgaris
reynaudii (Melo & Sauer, 1998, 1999). As this should
imply some difficulties in the estimation of fecundity,
attention was given to reveal atretic oocytes at different
phases of gonad development in L. gahi.
4. Stage with Latin numbers (i.e. maturity stage I)—to
describe maturity stages of the whole reproductive system.
In the present study, the nomenclature and classification
elaborated for L. bleekeri (Baeg et al., 1993) was used to
describe stages of oogenesis. Phases of ovary development
were after Melo & Sauer (1999), though their term ‘stage’
was changed into ‘phase’. Periods of oogenesis were after
Burukovsky et al. (1977), and female maturity stages were
assigned following Lipinski’s maturity scale (Lipinski, 1979).
RESULTS
MATERIAL AND METHODS
Oogenesis
Loligo gahi was sampled on board different fishing trawlers
and by r/v Dorada on the southeast Falkland shelf from June
1999 to February 2000. To study oogenesis, gonads of 12
females (98 to 165 mm ML) at various stages of maturity
were used. Ovaries were removed at sea and fixed in Bouin’s
solution, dehydrated and then embedded in paraffin. Histological sections (6–8 m thick) were cut and stained with
Mallory’s stain that distinguished the start of the yolk grain
appearance in oocytes (blue colour) in contrast to the pinkish
cytoplasm.
To estimate the level of oocyte resorption, reproductive
systems of 136 immature, maturing and mature females of
80–300 mm were preserved in 6% formaldehyde. From each
ovary, a random sample of 300–500 oocytes was studied
ashore. A total of 56,403 oocytes were assigned as ‘normal’ or
‘atretic’. Oocytes at the last stages of degeneration sometimes
might be confused with atretic empty follicles, although the
latter were rare. Thus, the confusion of the latest degenerating oocytes with atretic follicles was considered to be
unlikely.
The whole process of the squid maturation can be investigated in three levels:
1. Oogenesis—individual development of the oocytes into
ripe eggs.
2. Gonad development—histological changes in the ovary
during its growth and maturation.
3. Reproductive system maturation—changes of the whole
reproductive system including accessory glands.
A few different scales have been elaborated for each of
these levels (Burukovsky & Vovk, 1974;l Sauer & Lipinski,
1990; Baeg et al., 1993; Melo & Sauer, 1999) that provoked
significant confusion, particularly because in different papers
the same word (Stage or Phase) was used to describe either
oogenesis or ovary development. To avoid ambiguity, we
suggest use of the following terminology:
1. Stage with Arabic numbers (i.e. Stage 1)—to describe
stages of the oogenesis
2. Period—to describe intervals of oocyte development in
the oogenesis
3. Phase with Latin numbers (i.e. Phase I)—to describe
phases of the ovary maturation
Eight stages of oocytes were found with the first seven
seen on histological sections. Ripe eggs were unfortunately not found on the sections, and their description
was made from formaldehyde preserved ovaries. No
primary oogonia were found.
Period of oogonium production
Stage 1. Secondary oogonia (Fig.1A). These either secondary oogonia or pre-meiotic oocytes (probably a
mixture of both cellular stages) were ca. 20–30 m in
the long axis with a nucleus of 13–19 m.
Period of protoplasmic growth
Stage 2. Primary growth (Fig. 1A). Oocyte size varies
from 50 to 120 m in the long axis. The diameter of
centrally located nuclei increases from 30 to 70 m.
The nuclei possess one or several nucleoli of 4–6.5 m.
A few squamous follicular cells are attached to the
oocytes, their diameter being 6–7 m. Upon oocyte
growth they begin to multiply forming the follicular
cap.
Stage 3. Follicle cell multiplication (simple follicle)
(Fig. 1B) Oocyte size is about 180–300 m in the long
axis. The nucleus shifts to the animal pole, its diameter
attaining 100–120 m. Follicle cells become columnar
with the long diameter of 6–11 m. They increase in
numbers and surround the oocyte completely.
Interstitial period
Stage 4. Early yolkless (Fig. 1C) Oocyte size is about
250–400 m. The nucleus is of 100–130 m, nucleoli
are sometimes seen. The follicular epithelium begins to
penetrate into the oocyte, forming follicular folds. Follicle cells are of 9–11 m. The nucleus is at the future
animal pole.
Stage 5 Late yolkless (Fig. 1D) Oocyte size is of
500–800 m. The nucleus stops its growth, attaining
110–140 m. Folds of the follicular epithelium penetrate very deeply inside the cytoplasm occupying most
476
OOGENESIS AND GONAD DEVELOPMENT IN LOLIGO GAHI
Figure 1. Oogenesis in Loligo gahi. A. Secondary oogonia (so) and primary oocytes (po), scale bar 50 m; B. Follicle cell multiplication, scale
bar 100 m; C. Early yolkless oocyte, scale bar 100 m; D. Late yolkless oocyte, scale bar 100 m; E. Early vitellogenesis, scale bar 200 m;
F. Late vitellogenesis, scale bar 500 m.
477
V.V. LAPTIKHOVSKY & A.I. ARKHIPKIN
of the oocyte volume. No blue-stained yolk bodies are
present. A follicular syncytium is formed with follicle
cell nuclei containing several nucleoli (Fig. 2D).
Period of trophoplasmic growth
Stage 6. Early vitellogenesis (Fig. 1E). The oocyte size
is 1000–1300 m. Blue-stained yolk bodies appear and
are distributed randomly within the oocyte. Folds of
follicular epithelium occupy most of the oocyte volume.
Stage 7. Late vitellogenesis (Fig. 1F). The minimum
oocyte size is 1600 m in the long axis. Oocyte volume
increases due to yolk accumulation. The follicular syncytium starts to reduce towards the oocyte periphery.
Follicular folds occupy less than a half of the oocyte
volume.
Stage 8. Ripe egg. The ripe eggs are ovoid and of
bright-yellow colour. Their size varied from 1.4 1.9
to 1.8 2.8 mm, being mostly 1.6–1.8 2.2–2.7. Eggs
weight varied from 2.5 to 7.0 mg.
Phases of gonad development
Only five phases of ovary development were found in
our samples. Phase VII was doubtful, and phase I and
VIII were never encountered.
Phase II (Fig. 2A, Table 1). The most advanced
oocytes are at stage 3. The follicular epithelium surrounds its whole surface. Oocytes at the primary growth
stage are abundant, and a few oogonia are present.
Phase III (Fig. 2B, Table 1). The most advanced
oocytes are at the early yolkless stage (stage 4). The
oocytes at stage 3 predominate, those at stage 2 are
abundant and oogonia are still present.
Phase IV (Fig. 2C, Table 1). The most advanced
oocytes are at the late yolkless stage (stage 5). Oogonia
are not present.
Phase V (Fig. 2E, Table 1). The most advanced
oocytes are at the early vitellogenetic stage (stage 6),
oocytes at the primary growth are still present. The
most abundant oocytes are at stage 3–5. No ovulated
ripe eggs were found.
Phase VI (Fig. 2F, Table 1). The most advanced
oocytes are at the late vitellogenetic stage (stage 7),
oocytes at the primary growth stage are absent. The
most abundant oocytes are at stages 6–7. Some ovulated ripe eggs were present in the ovary.
Occurrence of different phases of gonad
development at different maturity stages
The occurrence of different phases of gonad development at different maturity stages is shown in the
Table 1. Females at the maturity stage I have gonads at
Phases II or III. Folds of the follicular epithelium can
appear on the oocytes, but they are still shallow.
Females at the maturity stage II had the gonads at
phase IV, with visible accessory nidamental glands.
Yolk accumulation in the oocytes begins at the maturity stage 3 (phase V), however most oocytes are still at
stages 3 to 5. When ripe eggs begin to ovulate and accumulate in the oviduct, the female is at the maturity
stage IV, and then at stage V, her gonad attains phase
VI. At this maturity stage, most of the oocytes accumulate yolk, although a few of them are still at stages 3–5.
Unfortunately, we had no opportunity to investigate
ovaries of partially and fully spent squid (phases
VII–VIII).
Table 1. Maturational changes during the ovary development in female L. gahi (ML—mantle length,
mm, MS—maturity stage, OP—phase of ovary development, N-number of assigned oocytes).
Stage of oocyte development, %
ML
MS
OP
N
1
2
3
98
96
104
90
101
110
110
125
12.5
120
110
165
I
I
I
II
II
II
II
III
III
V
V
V*
II
III
III
IV
III
IV
IV
V
V
VI
VI
VII(?)
46
93
72
34
11
84
66
68
58
15
42
73
2.2
2.1
39.1
36.6
6.9
14.7
58.7
52.7
58.3
14.7
29.8
40.9
4.4
12.1
10.7
24.2
35.3
15.5
20
2.4
12.3
4
8.6
34.7
61.8
100
25.0
28.8
29.4
24.1
6.7
2.4
13.7
5
6
7
8.8
13.8
46.6
50
20.6
2.9
6.9
20
28.5
35.6
8.8
34.5
4.5
19.1
27.6
6.7
16.7
16.4
1.5
* advanced partially spent female with spermatophores inside of the mantle cavity
478
resorption
1.4
OOGENESIS AND GONAD DEVELOPMENT IN LOLIGO GAHI
Figure 2. Ovary development. A. Phase II. B. Phase III. C. Phase IV. D. Follicular syncytium. E. Phase V. F. Phase VI.
479
V.V. LAPTIKHOVSKY & A.I. ARKHIPKIN
Oocyte resorption during oogenesis
A small number of atretic oocytes (0.8% of all oocytes
counted in mature females) were noted in most mature
squids (Table 2, Fig 3) whose oviducts were full of ripe
eggs. Among the total of 444 atretic oocytes studied,
only 2 were at the period of protoplasmic growth, and
the rest were yolk oocytes. One atretic protoplasmic
oocyte was found during examination of immature
ovaries preserved in formaldehyde, and another one
was found histologically.
The atretic protoplasmic oocyte in the formalin-preserved ovary was almost opaque, with a disintegrated
nucleus and vacuolated cytoplasm. That from the histological section had a nucleus without any inner structure and highly grainy cytoplasm (Fig. 3A).
Atretic yolk oocytes in formaldehyde preserved
gonads were of the same length as normal oocytes, but
looked like long, often curved sticks with thickened follicular epithelium. At the latest stages of degeneration
they became lead-life. An atretic oocyte (Fig. 3B) found
in the histological section of a post-spawning ovary
had the hypertrophic follicular layer still surrounding
the oocyte, and intensively vacuolated cytoplasm.
DISCUSSION
Generally, the process of oocyte development in the
gonad and number of oogenesis stages in L. gahi are
practically the same as described before for a number
of temperate loliginids (Yung, 1930; Konopacki, 1933;
Burukovsky & Vovk, 1974; Knipe & Beeman, 1978;
Lum-Kong, 1993; Sauer & Lipinski, 1990; Baeg et al.,
1993). However, it is rather difficult to make a comparative analysis of the oogenesis among the loliginids
studied, because different authors presented their
material differently, measuring and describing oocytes
in various ways. For example, our attempts to estimate
the nucleus size from published photographs showed
that all loliginids have an egg nucleus of about 140–180
Table 2. Frequency of occurrence of atretic oocytes (R, %) in female ovaries and their
percentage (P, %) at the different maturity stage and in the different seasons
Maturity stage
R, %
P, %
I
II
III
IV
V (winter, prespawning)
V (spring-summer, prespawning)
V (spring-summer, spawning)
VI (spring, partially spent)
0
0
0
0
37.5
80.9
89.5
75%
0
0
0
0
0.09
1.19
1.16
1.14
Figure 3. Oocyte resorption. A. Protoplasmic atretic oocyte. B. Yolk atretic oocyte.
480
N, female
4
5
14
11
16
63
19
4
N, oocyte
296
3082
1027
4698
10650
28510
6999
1141
OOGENESIS AND GONAD DEVELOPMENT IN LOLIGO GAHI
m, excluding L. pealei (50–90 m; Burukovsky &
Vovk, 1974).
However, the rate of the oocyte development and
therefore the proportions of different oocyte stages at
different maturity stages in L. gahi differs from that of
temperate loliginids whose females mature usually at
larger sizes (170–250 mm ML) than in L. gahi (120–160
mm ML) (Roper et al., 1984). Immature L. gahi at
maturity stage I (96–104 mm ML) had oocytes at early
yolkless stage (stage 4), whereas in L. bleekeri these
oocytes appeared at maturity stage II and in larger
squid ( 173 mm ML) (Baeg et al., 1993), similar to
L. pealei—at 120–190 mm ML (Burukovsky & Vovk,
1974). Early yolkless oocytes appeared at maturity
stage II in L. vulgaris reynaudii, but their proportion
(14%) is much lower than in L. gahi (35–100%) (Sauer
& Lipinski, 1990).
Vitellogenic oocytes also appeared earlier and in
animals of smaller sizes in L. gahi than in temperate
loliginids. Yolk accumulation in oocytes of L. bleekeri
started in maturing squid 177 mm ML (Baeg et al.,
1993), whereas in L. gahi maturing females (125 mm
ML) at maturity stage III had already 11–20% of
vitellogenic oocytes. Maturing females of L. vulgaris
reynaudii also had vitellogenic oocytes at maturity stage
III, but again their proportion (10%) was much lower
than that in L. gahi (Sauer & Lipinski, 1990).
The disappearance of small oocytes belonging to
early stages from the gonad of L. gahi seems to be quite
similar to other loliginids studied. In all of them,
oocytes of the primary growth (stage 2) are observed
up to the maturity stage III inclusive. In mature gonad,
oocytes at the simple follicle stage (3) are still present
although in smaller numbers (10–15%) (Burukovsky
& Vovk, 1974; Knipe & Beeman, 1978; Sauer & Lipinski, 1990; Baeg et al., 1993; Melo & Sauer, 1999).
Previously, earlier gonad maturation in cold water
squid (comparative to reproductive system maturation
maturity stages) has been shown for the temperate
ommastrephid squid Illex spp. (Burukovsky et al.,
1984; Laptikhovsky & Nigmatullin, 1992) in contrast
to the tropical species of the same family Sthenoteuthis
pteropus (Burukovsky et al., 1977). In our opinion,
study of a larger number of loliginid species by one
methodology is needed for the further investigation of
this phenomenon.
Oocyte resorption in the gonad of mature females
before and during spawning was found in the Loligo
vulgaris reynaudii (Melo & Sauer, 1998), as well as in the
gonatid squid Berryteuthis magister (Nigmatullin et al.,
1996), and in cold water octopodids (Laptikhovsky,
1999). In L. gahi, this phenomenon seems to be of
secondary importance since only a low number of
atretic oocytes were found. In contrast to L. v.reynaudii
that has multiple spawning events and, presumably,
oocyte resorption (Melo & Sauer, 1998, 1999), the
spawning season of L. gahi is short (Hatfield, 1996),
and probably only two egg batches are laid (Laptikhovsky et al., submitted). In this case, the oocyte
resorption loses its importance (or never has been) as
a tool to increase the actual fecundity by providing
additional nutrients from atretic oocytes to complete
maturation of the advanced oocytes.
Thus, the results of this study show that cold ambient
temperatures do not have any effect on the process of
oogenesis and gonad development, which seems quite
similar in all loliginid squid studied. However, cold
temperatures do affect the rates of oocyte development
and yolk accumulation. In the case of the cold water
L. gahi, both processes are shifted to the earlier stages
of reproductive system development; this probably
gives more time for the yolk accumulation at low
metabolic rates. Evolutionary acquisition of early
oocyte development together with other reproductive
adaptations (among them egg capsules with small
number of eggs, large eggs and hatchlings) enable
L. gahi to penetrate and successfully blossom in cold
subantarctic waters of the south-eastern part of the
Falkland shelf.
ACKNOWLEDGEMENTS
We gratefully acknowledge the scientific staff of the Falkland
Islands Government Fisheries Department for the creative
atmosphere and help at various stages of this study. We
thank the Director of Fisheries, John Barton, for supporting
this work.
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