By Kat Bolstad
Note: Kat (Tintenfisch) welcomes discussion in the Physiology & Biology forum of the TONMO.com Message Board.
The deep sea is the largest, yet least-explored habitat on Earth. Its seemingly adverse conditions include crushing pressure, total darkness, and temperatures near freezing, yet a spectacular variety of delicate and primitive life forms thrive in it. Most bizarre among these are the cephalopods, found from the deepest trenches to the ocean's very surface, burrowing into or hovering just off the sea bed, on and around deep-sea reefs, hydrothermal vents and cold seeps, adrift or swimming with great speed and agility through the water column. From evolutionary accidents to the pinnacles of success, the deep-sea cephalopod fauna exhibit fascinating physiological, morphological, and behavioral modifications.
Many deep-sea squids and octopi share certain general modifications such as gelatinous tissue (containing high concentrations of ammonium ions) which approximates the density of seawater, establishing neutral buoyancy and facilitating efficient locomotion (Villanueva et al. 1997); relatively large size; well-developed eyes that can detect any motion or light within the environment; and bioluminescence, which although more frequently observed in squid also occurs in several octopods and is thought to aid in prey capture, defense and countershading (Rees et al. 1998). Modified sucker structures can be found in several species of octopus (Stauroteuthis syrtensis suckers emit light and have lost the ability to grasp (Johnsen et al. 1999)) and squid (several squid families have developed chitinous hooks in addition to, as part of or replacing the standard sucker rings) (Fig. 1).
Figure 1. Mid-arm hooks and sucker rings on Mesonychoteuthis hamiltoni.
The cephalopod species in the deep sea represent several higher taxonomic groups, including the order Vampyromorpha, of which Vampyroteuthis infernalis is the sole recognized species. Its morphology intermediate between standard octopus and squid, V. infernalis merits its own order based on unique retractable sensory filaments (analogous to squid tentacles) found between arms I and II (dorsal and dorso-lateral). It inhabits the oxygen minimum layer of the world's temperate oceans (600-3000m), and has the lowest mass-specific metabolism rate recorded for any cephalopod, being able to respire and metabolize normally at 3% oxygen saturation. Like most deep-sea cephalopods, V. infernalis has very high gill surface areas, as well as high concentrations of hemocyanin in the blood. Specimens range from black to red in color (Seibel et al. 1998).
Cirrates are the most predominant octopod group found in the deep-sea habitat, and are generally small in comparison to octopod inhabitants of the photic zone. They range from 10 to 130cm total length (Villanueva et al. 1997), have anterior lateral fins on the mantle similar to those found on squid, and at least one species (S. syrtensis) is known to be bioluminescent. Cirrates lack ink sacs, have low fecundity and lay large eggs from which precocious young hatch after an extended brooding period. Bathypolypus, an Incirrate octopod, guards its eggs for 400 days, the longest recorded for any cephalopod (Wood et al. 1998).
As a group, deep-sea squid are also larger than their shallower counterparts, although many small-bodied species (ML < 10cm) are also found at great depth. The 'giant squid,' Architeuthis dux, is an extreme example of deep-sea gigantism, as are the cranchiids Mesonychoteuthis hamiltoni and Galiteuthis phyllura. The octopoteuthid Taningia danae, mastigoteuthid Idioteuthis cordiformis, and onychoteuthids Moroteuthis robusta and Kondakovia longimana also reach relatively gigantic sizes. Deep-sea squid are frequently transparent in life, the tissues turning opaque shortly after death; the eyes tend to be very highly developed, with relatively enormous lobes of the brain dedicated to their control, and may be inordinately large, set on stalks, or of markedly unequal size; photophores and other methods of bioluminescence are not uncommon; and the gills, with relatively large surface areas and thin blood-water transport barriers (1.01-3.34 µ) are extremely efficient but accordingly also very fragile (Seibel et al. 1997).
A variety of deep-sea cephalopods attain 'gigantic' size (dorsal mantle length, DML, > 1m). The largest known octopus, Haliphron atlanticus (Video link: Haliphron atlanticus), attains estimated total lengths of 4m and weights of 75kg. It is generally a tropical to sub-tropical species, with adults ranging into New Zealand waters, and is found from the surface to 3180m depth, though nowhere in great numbers. Its tissues are highly gelatinous and it is thought to reside primarily on or near the bottom. Limited stomach contents recorded to date suggest its primary prey to be cnidarians (O'Shea, in press).
Architeuthis dux, the giant squid (Fig. 2), reaches a maximum DML of 2.25m, total length of 13m (making it the longest recorded squid), and its size and highly ammoniacal tissues seem to have effectively deterred all predators save the sperm whale, Physeter catodon. However, its superlative size appears at odds with its internal anatomy - all food must reach the gut through the esophagus, 1m+ in length in adult specimens, of a maximum relaxed diameter 10mm, and passing directly through the brain. Additionally, though no adult giant squid has ever been seen live, it is believed to be a passive predator, suspended motionless in the water column at a 45° angle above its locked-together, vertically descending tentacles, waiting for fish or other small squid to swim within reach. The genus Architeuthis contains the single cosmopolitan species A. dux and adults are found throughout the temperate oceans at depths of 400-600m.
Figure 2. A mature female giant squid, Architeuthis dux.
Mesonychoteuthis hamiltoni, the colossal squid (Fig. 3), is believed by contrast to be a very active and highly aggressive predator. The largest recorded specimen (of the seven known to science) was 2.5m in mantle length, with a total length of 5.4m. While significantly shorter in total length than Architeuthis, the bodily proportions differ considerably and Mesonychoteuthis is far more massive in the head and mantle than a giant squid of the same total length. One specimen was recorded live at the surface in the Ross Sea in Antarctica, attacking Patagonian Toothfish of lengths up to 2m. Mesonychoteuthis is equipped with swiveling hooks on the tentacle clubs and an additional 8-18 biserial hooks in the middle portions of each arm (pers. obs.). It is known only from the Antarctic but is thought to occur throughout the water column from 2200m to the surface, and makes up 77% by weight of bull sperm whales' diet in the area (Clarke 1980). Scars found on the heads of sperm whales with Mesonychoteuthis beaks in their stomachs have been tentatively attributed to the squid's formidable hooks, suggesting a capacity for inflicting serious injury if threatened.
Figure 3. A submature female colossal squid, Mesonychoteuthis hamiltoni.
Another large squid, thought to reach total lengths of at least 8 m and tentatively placed into the family Magnapinnidae, has been observed and, on occasion, filmed by eight independent scientists in the Gulf of Mexico, Pacific, Atlantic and Indian Oceans. No specimen has ever been captured and the species is known to science from brief glimpses only. The animal possesses relatively enormous fins and its arms trail behind it, held out from the body on what appear to be rigid sections of arm terminating in elbow-like joints (Video link: Magnapinnidae).
Figure 4. Photophores on the ventral eye surface of Pterygioteuthis sp.
The diversity of bioluminescent organs found in deep-sea fish, molluscs, protozoans, coelenterates and chaetognaths indicates that this phenomenon has evolved separately on many occasions. Rees et al. (1998) suggest therefore that bioluminescence is a specialized function of compounds found in all organisms, having evolved in much the same manner in each instance but diversifying into a wide range of structures and mechanisms.
Luciferases, the enzymes that act upon luciferins (the substrates oxidized to produce light in bioluminescent organisms) are thought to have evolved from mixed-function oxygenases. Luciferins utilize oxygen compounds extremely efficiently to denature free radicals and are most commonly found in areas of high free radical concentration including the skin, gut and gonads. It is thought that while organisms in the aphotic zone are frequently exposed to deleterious oxygen compounds, they are overall at less risk due to free radicals because of the absence of light irradiance. The luciferases therefore, less critical in oxidizing free radicals, and unnecessary for anaerobic metabolism, began to develop into the beneficial light-producing compounds found today in bioluminescent organisms (Rees et al. 1998).
Nearly all marine bioluminescence is blue-green light within the range of 470-490 nm, the optimum wavelengths for transmission through seawater (Rees et al. 1998). Luminescence of different colors is impractical as shorter and longer wavelengths are soon absorbed. Studies on the firefly squid, Watasenia scintillans, have shown that the eyes of deep-sea squid are most sensitive to the blue-green light produced by bioluminescent organisms, and that a combination of retinal thickenings and three separate visual pigments may even allow the firefly squid enough sensitivity to distinguish between species due to slight wavelength differences (Matsui et al. 1988, Michinomae et al. 1994). It has also been shown that parolfactory vesicles in deep-sea species of Loligo are photoreceptive (Messenger 1967).
Figure 5. Photophores on an arm of Cheiroteuthis sp.
Bioluminescence in deep-sea cephalopods is generally considered to aid primarily in feeding and defense, rather than reproduction or communication. Extended periods of luminescence put organisms at risk of predation, and observed displays are often limited to brief patterns or flashes of light. Some species, such as the octopus S. syrtensis, have unique patterns, but these are scattered and distorted within a short distance and would serve little function as a communication tool. In addition, the highly developed eyes and strong affinity of deep-sea crustaceans for light make prey-luring a likely function of bioluminescence (Johnsen 1999).
Figure 6. Photophore on the ventral eye surface of Cheiroteuthis sp.
Cephalopod bioluminescence takes several forms - it may be generated in photophores (light-emitting organs permanently located on the external or internal surfaces of the animal) (Figs 4-6), pockets of bacteria covered or uncovered as necessary, or in secretions. One of the best-known bioluminescent squid, Taningia danae, carries the largest photophores in the animal kingdom - lemon-shaped organs up to 5cm in length - in the tips of its second (dorso-lateral) arms. These have been observed to flash rapidly when the animal is threatened, and on one occasion the display was observed coupled with an aggressive attack (Wood 2003). However, most known specimens of T. danae have been taken from the stomachs of predators including sharks, tuna, albatross, elephant seals, and sperm whales. As these animals are largely non-visual hunters and therefore unlikely to be affected by the luminescent display, the effectiveness of this response in confusing or discouraging them is doubtful.
Some squid, such as Heteroteuthis dispar, can secrete bioluminescent mucous from glands adjacent to the ink sac. Akin to the black ink-clouds released by photic zone inhabitants, the glowing cloud is assumed to blind and / or confuse predators long enough for the squid to escape (fide Young 1977).
Hunting and predator-avoidance strategies in the deep sea differ markedly from those in the photic zone. Without light, and assuming prey are not constantly bioluminescent, visual hunting is a rarity and long stretches of chase/avoidance swimming are unnecessary. Predators frequently utilize the sit-and-wait technique, resulting in most animals needing only brief avoidance/threat responses. This less active lifestyle coincides with the development of fatty tissue in higher proportions than those found in related shallow-water species, aiding in neutral buoyancy and reducing the energy expended in maintaining musculature. In an environment where long stretches of chase or avoidance swimming are highly uncommon and anaerobic metabolism becomes unnecessary, most cephalopods have reduced metabolism rates, distributing energy more efficiently and requiring less food intake on the whole.
Seibel et al. (1997) measured the metabolism rates of 33 cephalopod species and determined not only that metabolism rates decrease with depth (the extreme example being V. infernalis, which can function normally at oxygen partial pressures of 3), but also that cephalopods have more extreme metabolism trends than fish or crustaceans, due to their highly active lifestyles within the photic zone and efficient modification for life in the deep sea.
The difficulties in observing deep-sea animals live in situ leave scientists with a regrettable dearth of information on normal behaviors.
Villanueva et al. (1997) recorded and classified the swimming and crawling gaits of ten unidentified cirrate octopod species on the Mid-Atlantic Ridge. The cirrates were observed resting on the sea floor, crawling using the arms symmetrically, propelling themselves upwards in response to threat, drifting slowly on deep-sea currents, swimming using peristaltic mantle pumping, and swimming using the lateral fins (probably most efficient) (Video link: Cephalopod gaits). Vampire squid also swim primarily using their lateral fins; throughout the lifespan ontogeny of the animal, however, the fins change size and position, modifying the gait for greater efficiency as the animal's surface area to volume ratio decreases with growth (Seibel et al. 1998).
Villanueva et al. (1997) also observed cirrate threat responses to the approach of the submersible and recording equipment. These behaviors also differ from threat responses in shallow-water octopods; as deep-water species lack ink sacs and swim more slowly, those unable to escape through locomotion exhibit two main stationary threat responses. In the 'ballooning response' the individual fills the webbing between individual arms with water, increasing its overall size. Animals can control each section of the webbing individually and may inflate one, several or all simultaneously. During the second response, the 'pumpkin posture,' the animal closes the entire webbing spherically below its ventral surface, also increasing its size substantially and presumably making predation more difficult.
Low metabolism, scarcity of mates, and low productivity of the surrounding habitat all affect the reproductive behaviors of deep-sea cephalopods. The chance to mate may occur only once or not at all, and the resulting production and, in some species, guarding of egg clutches poses an additional challenge. These considerations make reproduction the single largest energy-expensive event in the organism's lifetime.
Actual reproductive behaviors are mostly subject to hypothesis and speculation in the absence of observations or evidence. It is known that the males of some cephalopod species transfer sperm to the female using a large organ protruding from the mantle (the penis) while others use a modified arm (the hectocotylus). Simple sperm are stored in packets called spermatophores, which may be placed inside the female's mantle, hydraulically implanted into her mantle, arms, head, or around the beak, or may be jettisoned along with the entire hectocotylus in the female's general direction. It is also not uncommon to find male squid specimens (e.g. Architeuthis dux) bearing implanted spermatophores, which may be from other males or may be self-implanted during the trauma of capture.
Female deep-sea octopi generally store the spermatophores until the eggs are produced, then simultaneously fertilize and lay a relatively small clutch of large eggs. The precocious young hatch after an extending brooding period (up to 400 days in some species), during which the mother guards the clutch, aerating the eggs and fending off predators. The female ceases eating shortly after the clutch is laid and dies when the eggs hatch (Wood et al. 1998).
Female squid also expend the entirety of their energy in reproduction. Although most do not brood their clutches (some exceptions being species of the family Gonatidae, and possibly some species of the genera Moroteuthis and Teuthowenia), by the time the eggs are laid the females are often degenerate, lacking arms, tentacles, and sometimes fins. It is thought that most die within hours of spawning.
OUR LIMITED KNOWLEDGE
The same conditions that give rise to the wonders of deep-sea life also unfortunately hinder the efforts of scientists studying them. In situ observations are complicated by the light, turbulence and noise necessarily accompanying submersibles and photographic devices. The intrusion of research equipment into the animals' otherwise unchanging habitat almost certainly affects their behavior; it is possible that no behavioral observations made to date have recorded anything more than threat-responses stimulated by the intrusion of our awkward and cumbersome deep sea technology. Maintenance and development of this technology also present an obstacle to researchers - justification of deep-sea research in terms of time and expense is made challenging by the uncertainty of encountering subjects for observation due to disturbance and the animals' scarcity. Once subjects are encountered, identification by simple observation is often impossible since distinguishing characters are often internal, including the shell (gladius), gills, and genital apparatus. Collection of specimens is imprecise and risky, as unwieldy mechanical collection devices often damage and destroy the soft-tissued subjects (Villanueva et al. 1997). Specimens captured in fishing nets frequently suffer extensive damage and bioluminescent organisms brought to the surface have often expended their luminescence in extended threat responses.
Captive research and ongrowth present another problem; even the best aquaculture and laboratory facilities differ greatly from the deep-sea environment, and captive-observed behaviors are almost certainly altered. Feeding behaviors will be dictated by the food available, reproductive behaviors by the artificial conditions (e.g. presence / absence of mates, differences between captive habitat and natural spawning grounds), brooding behaviors by the absence of potential predators. In short, while dry-land research holds certain advantages over in situ observations (the chance to record life histories, for example), only a combination of the two can form a complete insight into the mysteries of cephalopod life in the deep sea.
In order to continue research on deep-sea cephalopods, efforts should be made to develop technology that will be less intrusive or at least less obtrusive during observations. Collection of live adult specimens, although methods are under constant refinement, is still semi-impractical as their delicate tissues are easily destroyed. Emphasis should also be placed on developing protocols for captive ongrowth of deep-sea species, as the juveniles are frequently found in the surface layers of the ocean and in far greater abundance than the adults.
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Last updated: 5/6/03