Egg masses of flying squids (cephalopoda: ommastrephidae).
KEY WORDS: Cephalopod, egg mass, oceanic squid, pycnocline, squid spawning behavior
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, O'Dor 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 (O'Dor et al. 1982a, Sakurai et al. 2000). Posternbryonic 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 observations 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, O'Dor et al. 1980, 1982a, O'Dor & 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 (O'Dor et al. 1982a, Balch et al. 1985, O'Dor & Balch 1985), and various reviews (Okutani 1983, Boyle & Rodhouse 2005, O'Dor & 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 2-1 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. 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 nidamental 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). O'Dor 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 locomotion (jet propulsion), is used to pump the egg mass constituents. 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 distributed 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).
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 O'Dor 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 Todarodespacificus 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 1 (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 (O'Dor & 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 (O'Dor & Balch 1985, von Boletzky 1998, O'Shea et al. 2004). Even in captive experiments, it is difficult to catch the egg mass because a small pressure wave pushes them aside (O'Dor & Balch 1985, Puneeta et al. 2015).
The specific gravity of individual eggs is slightly denser than that of seawater (1.10 for Illex illecebrosus; O'Dor & 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. O'Dor and Balch (1985) calculated the initial density of the egg mass of I. illecebrosus to be 0.03 o, units higher than the water from which it is formed. Consequently, the egg mass inevitably sinks following 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 (O'Dor & 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 (O'Dor & 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 (O'Dor & Balch 1985). For an Illex egg mass, the thermal diffusivity (heat transfer) is 0.0036 cm2/sec, which means that the average temperature of egg mass is 90% equilibrated in about 10 h (O'Dor & Balch 1985). Diffusion of ions (chemical equilibration) into the mass may take days, due to the thick outer jelly, which acts as a barrier (O'Dor & Balch 1985, 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 embryos (O'Dor et al. 1982b, Sakuraietal. 1996, Staafet 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 (O'Dor et al. 1982b, Vijai et al. 2015b).
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 distribution 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 embryonic 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 Reynold's numbers (Blake 1983, O'Dor & Balch 1985). The large quantity of gel ensures a protective and sterile environment for the developing embryo (O'Dor 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, O'Shea et al. 2004). When egg masses are broken under 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.
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 invertebrate 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 (O'Dor 1983). Determining the relationships between egg mass data and oceanographic parameters will improve our ability to predict spawning events and associated abiotic factors (O'Dor 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 requires 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 (Ommastrephinae) 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.
I thank Pandey Puneeta and Erica A. G. Vidal for comments on the manuscript.
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DHARMAMONY VIJAI *
Oceanography Division, Tohoku National Fisheries Research Institute, Japan Fisheries Research and Education Agency, 25-259 Samemachi, Hachinohe, 031-0841, Japan
* Corresponding author. E-mail: email@example.com
TABLE 1. Ommastrephid egg masses observed in the wild and the depths at which they were encountered. Depth Species Number (m) Location Illex coindetii 1 Surface Naples, Mediterranean Coast of Italy Sthenoteuthis 1 22-32 Tropical eastern Atlantic pteropus 3[degrees] S 6[degrees] 30' W Nototodarus gouldi 9 10-30 Poor Knights Islands, Bay of Islands, New Zealand Dosidicus gigas 1 16 Guaymas Basin, Gulf of California, bottom depth [approximately equal to] 1,800 m 6 9-14 Guaymas Basin, Gulf of California, bottom depth [approximately equal to] 2,000 m Unidentified 1 22 Fethiye, Mediterranean Coast (Ommastrephes of Turkey bartramii?) Species Number Source Illex coindetii 1 Naef (1928) identified by von Boletzky et al. (1973) Sthenoteuthis 1 Laptikhovsky and Murzov (1990) pteropus Nototodarus gouldi 9 O'Shea et al. (2004) Dosidicus gigas 1 Staaf et al. (2008) 6 Birk et al. (2016) Unidentified 1 Lee (2015), Tannover (2015) (Ommastrephes bartramii?)
Please note: Some tables or figures were omitted from this article.
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|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2016|
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