Egg Masses of Flying Squids (Cephalopoda: Ommastrephidae)

Abstract

Ommastrephid squids have a pelagic lifestyle, with reproductive behavior that is characterized by the extrusion of fragile, neutrally buoyant egg masses, the release of paralarvae into the surface plankton, and the use of large-scale current patterns for larval transport, leading to the assisted migration of populations. Although the exact process of egg mass formation is unknown, the most accepted hypothesis suggests that, at spawning, eggs are first coated with oviducal gland secretion and released with nidamental gland secretions. Subsequently, the eggs mix with broken spermatophores or spermatangia for fertilization. The fertilized eggs are then extruded into the seawater to form a globular mass. These neutrally buoyant gelatinous egg masses are thought to maintain their location in the water column by floating at the interface between water layers of slightly different densities (above the pycnocline). The embryos develop within a favorable temperature range. Once hatched, the paralarvae leave the egg mass and swim to the surface. This review assimilates and assesses all available literature on the egg masses of ommastrephid squids. The data presented here clearly show how fragmentary our knowledge is about this important reproductive stage. Thus, increased efforts are required to develop observation and sampling techniques in the wild to obtain more direct evidence about reproduction in squids.

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Egg Masses of Flying Squids (Cephalopoda: Ommastrephidae)
Author(s): Dharmamony Vijai
Source: Journal of Shellfish Research, 35(4):1007-1012.
Published By: National Shellfisheries Association
DOI: http://dx.doi.org/10.2983/035.035.0423
URL: http://www.bioone.org/doi/full/10.2983/035.035.0423
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EGG MASSES OF FLYING SQUIDS (CEPHALOPODA: OMMASTREPHIDAE)
DHARMAMONY VIJAI*
Oceanography Division, Tohoku National Fisheries Research Institute, Japan Fisheries Research and
Education Agency, 25-259 Samemachi, Hachinohe, 031-0841, Japan
ABSTRACT Ommastrephid squids have a pelagic lifestyle, with reproductive behavior that is characterized by the extrusion of
fragile, neutrally buoyant egg masses, the release of paralarvae into the surface plankton, and the use of large-scale current
patterns for larval transport, leading to the assisted migration of populations. Although the exact process of egg mass formation is
unknown, the most accepted hypothesis suggests that, at spawning, eggs are first coated with oviducal gland secretion and released
with nidamental gland secretions. Subsequently, the eggs mix with broken spermatophores or spermatangia for fertilization. The
fertilized eggs are then extruded into the seawater to form a globular mass. These neutrally buoyant gelatinous egg masses are
thought to maintain their location in the water column by floating at the interface between water layers of slightly different
densities (above the pycnocline). The embryos develop within a favorable temperature range. Once hatched, the paralarvae leave
the egg mass and swim to the surface. This review assimilates and assesses all available literature on the egg masses of
ommastrephid squids. The data presented here clearly show how fragmentary our knowledge is about this important reproductive
stage. Thus, increased efforts are required to develop observation and sampling techniques in the wild to obtain more direct
evidence about reproduction in squids.
KEY WORDS: Cephalopod, egg mass, oceanic squid, pycnocline, squid spawning behavior
INTRODUCTION
In both cuttlefish (Sepioidea) and squids (Teuthoidea), the
oocytes develop from the branching of the genital strand
(inside ovary), which almost extends to the posterior end of
the mantle from the posterior end of the stomach, within the
viscero-pericardial coelom (Harman et al. 1989). The first
envelope of the oocyte is the chorion, which is secreted by the
follicle during late oogenesis (von Boletzky 1989). Mature
oocytes (ova) of teuthoids break free from the follicular complex
and accumulate in the oviducts (von Boletzky 1986, Nigmatullin
et al. 1995). In parallel to oocytes accumulating in the oviducts,
the nidamental and oviducal glands develop (Nigmatullin et al.
1995). Once the oviducts are full of ova, the ova are either
released individually or in successive series of several to many
eggs at a time (von Boletzky 1986). During egg laying, each egg
cell and its chorion is surrounded by some jelly. An inner layer
of jelly is first provided by the oviducal gland, after which the
nidamental glands add an outer layer of jelly (von Boletzky
1989). Each egg is individually enveloped in Sepioidea, whereas
batches of eggs are encompassed within a sheet of nidamental
gland jelly in most Teuthoidea (Natsukari 1970, OÕDor 1983,
Okutani 1983, Segawa 1987, von Boletzky 1989). During
spawning, eggs are fertilized by viable spermatozoids stored
inside the mantle cavity or the seminal receptacles of the female
located in the buccal membrane. As a result, mating and
spawning need not coincide (Harman et al. 1989, Nigmatullin
et al. 1995). Spermatozoa must cross some of the freshly secreted
jelly to reach the micropyle of the egg for successful fertilization
(von Boletzky 1989).
The reproductive system of a mature ommastrephid female
consists of a single ovary, paired oviducts, and oviducal and
nidamental glands. At spawning, females produce numerous
small eggs, encapsulated in gelatinous masses (OÕDor et al.
1982a, Sakurai et al. 2000). Postembryonic development is
achieved through a unique paralarval stage (Young & Harman
1988), which is known as rhynchoteuthion. This stage is
characterized by the tentacles fusing together to form a trunk-
like proboscis, with a few suckers on the distal tip (Roper et al.
2010).
von Boletzky (1986, 1989, 1998, 2003) has provided several
detailed reviews on cephalopod eggs and egg masses; however,
a comprehensive overview on ommastrephid egg masses is
lacking. Among the 22 ommastrephid squids (Roper et al.
2010), the egg masses of just 4 ommastrephids have been
reported in the wild (Table 1). Most of our knowledge on this
critical period of the life cycle is based on laboratory observa-
tions of experiments on captive Todarodes pacificus (Hamabe
1961a, 1961b, 1962, 1963, Bower & Sakurai 1996, Bower 1997,
Puneeta et al. 2015, 2016), Illex illecebrosus (Durward et al.
1980, OÕDor et al. 1980, 1982a, OÕDor & Balch 1985), Illex
coindetii (von Boletzky et al. 1973), Sthenoteuthis oualaniensis
(Cheslin & Giragosov 1993), and Dosidicus gigas (Staaf et al.
2008). This article provides an overview of existing information
on ommastrephid egg masses, including recent studies on the
structure, formation, and properties of these masses.
STRUCTURE AND FORMATION
The spawning of ommastrephids has never been observed
in nature. On the basis of observations of the spawning of
Todarodes pacificus in captivity (Hamabe 1962, Bower &
Sakurai 1996, Puneeta et al. 2015), Illex illecebrosus (OÕDor
et al. 1982a, Balch et al. 1985, OÕDor & Balch 1985), and various
reviews (Okutani 1983, Boyle & Rodhouse 2005, OÕDor &
Dawe 2013, Sakurai et al. 2013), the events during egg mass
formation have been hypothesized (Fig. 1). At spawning, water
enters the mantle cavity, mixes with the nidamental gland
secretion, and forms a jelly (Fig. 1A). This nidamental gland
jelly is expelled through the funnel to produce a gelatinous
envelope of about 2-l volume in the arm crown of the female to
form a wrapper or bed for the eggs that follow (Fig. 1B). Mature
ova released from the oviduct are wrapped with a gelling agent
from the oviducal gland using water to form a mucous matrix.
*Corresponding author. E-mail: keralavijai@yahoo.co.in
DOI: 10.2983/035.035.0423
Journal of Shellfish Research, Vol. 35, No. 4, 1007–1012, 2016.
1007

This mucous matrix is translocated to the buccal membrane
through the funnel, and a passage is formed between the two
ventral arms. The eggs might be fertilized there, after which the
mucous matrix is pumped into the gelatinous envelope formed
by the nidamental gland jelly (Fig. 1C). The female repeats this
process by continuously contracting its mantle to pump nida-
mental gland jelly and the mucous matrix. For species (e.g.,
Illex) where spermatophores are stored inside the mantle cavity,
mechanical activity mixes the eggs from the oviducts, the gelling
agents from the nidamental and oviducal glands, and the
broken spermatophores with water to form the substance of
the egg mass. These secretions accumulate and swell gradually
in front of the female to form a large egg mass (Fig. 2). OÕDor
et al. (1982a) describes the process as being ‘‘similar to blowing
up bubble gum.’’ The mobility of females is limited during
spawning because the funnel, which is usually used for loco-
motion (jet propulsion), is used to pump the egg mass constit-
uents. Consequently, females might sink through the epipelagic
zone during the inflating process.
The sequence of events in egg mass formation reported for
ommastrephids has also been proposed for other cephalopods
that form egg masses. Possible examples include Thysanoteuthis
rhombus (Nigmatullin et al. 1995; as part of a hypothesis) and
the Pygmy squid Idiosepius paradoxus (Kasugai & Ikeda
2003).
The reaction between the mucosubstance in the nidamental
gland and the surrounding seawater results in the formation of
an outer, water-soluble layer, which is devoid of eggs, and an
inner mucous matrix (Kimura et al. 2004). An egg mass of
80 cm diameter contains approximately 200,000 eggs (Bower &
Sakurai 1996, Puneeta et al. 2015). Individual eggs are distrib-
uted homogeneously inside the mucous matrix (Durward et al.
1980, Staaf et al. 2008, Puneeta et al. 2015). The inner matrix
consists of a fibril matrix in which the fertilized eggs are
arranged in a viscous watery substance (Bower & Sakurai
1996, Kimura et al. 2004). This network of fibrils might act as
a scaffold, facilitating the homogenous and discrete distribution
of eggs, and maintaining the overall shape of the egg mass
(Puneeta et al. 2015). The chorion surrounding each egg
expands as the embryo develops and gains size. Embryos within
the egg mass are oriented vertically, with their heads facing
downward (Staaf et al. 2008, Puneeta et al. 2015). Hatching
paralarvae spend approximately 2 h inside the egg mass before
swimming out (Puneeta et al. 2015). Once out of the egg mass,
the paralarvae slowly ascend vertically to the surface by hop-
and-sink swimming behavior (Bower & Sakurai 1996, Yoo et al.
2014, Puneeta et al. 2015).
TABLE 1.
Ommastrephid egg masses observed in the wild and the depths at which they were encountered.
Species Number Depth (m) Location Source
Illex coindetii 1 Surface Naples, Mediterranean Coast of Italy Naef (1928) identified by von Boletzky et al. (1973)
Sthenoteuthis pteropus 1 22–32 Tropical eastern Atlantic 3°S6°30#W Laptikhovsky and Murzov (1990)
Nototodarus gouldi 9 10–30 Poor Knights Islands, Bay of Islands,
New Zealand
OÕShea et al. (2004)
Dosidicus gigas 1 16 Guaymas Basin, Gulf of California,
bottom depth 1,800 m
Staaf et al. (2008)
6 9–14 Guaymas Basin, Gulf of California,
bottom depth 2,000 m
Birk et al. (2016)
Unidentified
(Ommastrephes
bartramii?)
1 22 Fethiye, Mediterranean Coast of Turkey Lee (2015), Tannover (2015)
Figure 1. Hypothesis of ommastrephid egg mass formation. Concepts are
adapted from Hamabe (1962), OÕDor et al. (1982a), Bower and Sakurai
(1996), Sakurai et al. (2003), and Puneeta et al. (2015). (A) Nidamental
gland secretion begins. (B) Nidamental gland jelly is expelled through the
funnel producing a gelatinous envelope in the arm crown of the female.
(C) Mature eggs released from the oviducts are wrapped with a gelling
agent from the oviducal gland. The eggs then pass through the funnel and
a passage that forms between the two ventral arms. The eggs are then
pumped into the gelatinous bulb, which was formed by the nidamental
gland jelly. Fertilization takes place inside the mantle cavity or at the
buccal region, by mixing the eggs with broken spermatophores. F, fin; ov,
ovary; od, oviduct; ng, nidamental gland; odg, oviducal gland; ngs,
nidamental gland secretion; 1, a mixture of nidamental gland secretion
and water expelled through the funnel; 2, secretion of the oviducal gland
with ripe eggs.
VIJAI1008

PROPERTIES
Egg masses that spawn in pelagic waters sink, and are
suspended in the mesopelagic zone (pycnocline) or in a layer
where their density matches that of the surrounding waters.
The properties of egg masses and their interaction with
surrounding oceanographic parameters (such as temperature,
salinity, and density) are not well investigated. Information on
this important aspect is limited to a single study conducted by
OÕDor and Balch (1985) on captive spawned Illex illecebrosus
egg masses.
The main constituent of egg masses is the water where they
are formed. The volume of the egg mass equated with their
biotic components (i.e., eggs, and nidamental and oviducal
jellies) clearly indicates that the egg mass consists greater than
99% seawater. For example, a few grams of Todarodes pacificus
eggs (oviduct weighing ;20–30 g) and a few milliliters of gland
secretions (nidamental and oviducal glands together weighing
;10–20 g) produce egg masses of ;1 m diameter, with a volume
of ;500 l (Puneeta et al. 2015). This watery body is naturally
transparent. This phenomenon coupled with their mesopelagic
distribution explains why egg masses have been rarely seen or
collected (OÕDor & Balch 1985). Because of the transparent
appearance and fragile nature of egg masses, divers might fail
to detect them, even if they swim through them. Moreover,
underwater cameras encounter the same problem. The gel is
too fragile to be retained in trawls or plankton nets (OÕDor &
Balch 1985, von Boletzky 1998, OÕShea et al. 2004). Even in
captive experiments, it is difficult to catch the egg mass because
a small pressure wave pushes them aside (OÕDor & Balch 1985,
Puneeta et al. 2015).
The specific gravity of individual eggs is slightly denser than
that of seawater (1.10 for Illex illecebrosus;OÕDor & Balch
1985). Jellies formed by the nidamental and oviducal glands are
viscous and denser than seawater, making the egg masses denser
than seawater where they form. OÕDor and Balch (1985)
calculated the initial density of the egg mass of I. illecebrosus
to be 0.03 s
t
units higher than the water from which it is
formed. Consequently, the egg mass inevitably sinks follow-
ing detachment from the ‘‘mother’’ squid. Sinking velocity is
determined by the drag coefficient, which, in turn, depends on
the size of the egg masses. For example, a 50-cm Illex egg mass
attains a terminal velocity of 1 m/min (OÕDor & Balch 1985).
Seawater density increases with depth, and the egg mass
becomes neutrally buoyant when it reaches in equilibrium
with the surrounding water, which tends to occur at/above
pycnoclines/thermoclines. Laboratory experiments (OÕDor &
Balch 1985, Puneeta et al. 2015) and wild observations
(Laptikhovsky & Murzov 1990, Birk et al. 2016) support this
assumption.
The fluid properties of the outer jelly and inner matrix of
the egg masses regulate the endurance of the egg masses and
facilitate embryo development. The difference in the density
between the egg mass and the surrounding water primarily
depends on the temperature and salinity of the water within
the egg masses. The rates of temperature and ionic equilibrium
determine how long a neutrally buoyant egg mass remains
suspended after an influx of denser water (OÕDor & Balch
1985). For an Illex egg mass, the thermal diffusivity (heat
transfer) is 0.0036 cm
2
/sec, which means that the average
temperature of egg mass is 90% equilibrated in about 10 h
(OÕDor & Balch 1985). Diffusion of ions (chemical equilibra-
tion) into the mass may take days, due to the thick outer jelly,
whichactsasabarrier(OÕDor&Balch1985,Woods&
DeSilets 1997). Successful development of the embryo and
hatching depends on prevailing oceanographic parameters,
particularly temperature. An ambient temperature range is
essential for the normal development of ommastrephid em-
bryos (OÕDor et al. 1982b, Sakurai et al. 1996, Staaf et al. 2011,
Vijai et al. 2015a, 2015b). Under low-temperature conditions,
undeveloped eggs might remain in stasis for a period of time
until the temperature increases (OÕDor et al. 1982b, Vijai et al.
2015b).
FUNCTIONS
In contrast to nearshore myopsids, oceanic oegopsids release
eggs individually or encapsulated within jelly into the open
water, because they do not have any substrate on which to
attach. The evolutionarily successful and cosmopolitan distri-
bution of the ommastrephid group indicates that the release of
eggs within egg masses is an optimal method for dispersal. To
understand the functions of the egg masses, the requirements of
a developing embryo should be identified. For normal embry-
onic development until hatching, an embryo mainly requires
(1) a decontaminated setting, (2) a steady oxygen supply,
(3) ambient temperature, (4) protection from predators, and
(5) a continual source of energy. As long as the embryos are
inside the egg masses, these requirements are fulfilled.
Hydrodynamically, the egg masses behave like rigid spheres
that are able to withstand relatively strong water currents over
an appropriate range of ReynoldÕs numbers (Blake 1983, OÕDor
& Balch 1985). The large quantity of gel ensures a protective
and sterile environment for the developing embryo (OÕDor et al.
1980). The outer nidamental gland jelly layer is effective in
preventing ciliates, crustaceans, protozoans, and bacteria from
infesting the egg masses (Durward et al. 1980, Bower & Sakurai
1996, OÕShea et al. 2004). When egg masses are broken under
Figure 2. Captive spawned egg mass of Todarodes pacificus (diameter:
80 cm; Puneeta et al. 2015).
EGG MASSES OF FLYING SQUIDS 1009

captive conditions, microbial invasion causes the mortality of
all embryos (Puneeta et al. 2015). Recent studies (Birk et al.
2016) have reported the presence of ciliate contamination, even
in the wild egg masses of Dosidicus gigas, giving clues about
their possible role as the first feeding items of squid paralarvae
(Vidal & Haimovici 1998).
The egg mass wall is not a barrier to oxygen diffusion. In
fact, oxygen gradients across the wall are negligible (Moran &
Woods 2007), guaranteeing sufficient oxygen circulation in the
inner mucous matrix. The inner mucous matrix functions as
a medium for the oviducal gland jelly, and is essential for
chorion expansion and the formation of the perivitelline space
around the ovum (Ikeda et al. 1993), which are required for the
normal embryonic development of the squid.
CONCLUSIONS
The data presented here clearly show how fragmentary our
knowledge remains about the important reproductive stage of
this squid group, despite it contributing to the largest inverte-
brate fishery in the world (Arkhipkin et al. 2015). Almost all
inferences are based on seasonal captive experiments and
occasional reports from the wild. Captive experiments should
be conducted on other members of this group to improve our
knowledge about egg mass characteristics. We know almost
nothing about actual spawning scenarios in the wild. An actual
spawning ground might contain thousands of egg masses for
a short duration. For commercial species, the spawning seasons
and areas are relatively well documented/predictable; thus,
these putative spawning areas could be targeted for blue-water
dives and remotely operated vehicle observations to gain
further insights, and obtain confirmatory evidence from the
natural environment. Improved methods for collecting recent
hatchlings and egg masses (which might reach >3 m diameter for
large species) are needed to improve our understanding about
their distribution in the ocean (OÕDor 1983). Determining the
relationships between egg mass data and oceanographic pa-
rameters will improve our ability to predict spawning events
and associated abiotic factors (OÕDor 1983). The outer layers of
the mass are permeable to oxygen, despite their strength and
durability to retain growing embryos for several days. Thus,
information is required to understand how these layers achieve
such high gas permeability, including closer ultrastructural
examination (Moran & Woods 2007).
Historically, knowledge about the feeding behavior of the
early stages of oceanic squids has been a major bottleneck for
the development of culture technology (Villanueva et al. 2014).
Discovery of ciliates in naturally spawned egg masses, which
might represent an early food source for hatchlings (Birk et al.
2016), warrants further exploration.
Comparison of the spawning sites and the early life history
of the nerito-oceanic and oceanic reproductive strategies re-
quires further investigation. In the nerito-oceanic (coastal)
strategy (e.g., Illicinae and Todarodinae), spawning occurs near
the bottom of the shelf and continental slope, or in the vicinity
of oceanic islands and underwater mountains (Nigmatullin &
Laptikhovsky 1994, Roper et al. 2010). Species (Ommastrephi-
nae) adapted to the true oceanic strategy spawn in open waters
(Nigmatullin & Laptikhovsky 1994, Vijai et al. 2014). Egg
masses either float in the near-bottom habitat or near the
surface, depending on the species (Roper et al. 2010). In
conclusion, comparison between the spawning behavior and
egg masses of ommastrephids with phylogenetically related and
ecologically similar oegopsids could provide new insights on
several features of squid biology that remain ambiguous.
ACKNOWLEDGMENT
I thank Pandey Puneeta and

Erica A. G. Vidal for comments
on the manuscript.
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