Cephalopod

Left: An octopus opening a container with a screw cap
Right: Hawaiian bobtail squid, Euprymna scolopes, burying itself in the sand, leaving only the eyes exposed

Cephalopods are widely regarded as the most intelligent of the invertebrates, and have well developed senses and large brains (larger than those of gastropods).[8] The nervous system of cephalopods is the most complex of the invertebrates[9][10] and their brain-to-body-mass ratio falls between that of endothermic and ectothermic vertebrates.[7]^:14 Captive cephalopods have also been known to climb out of their aquaria, maneuver a distance of the lab floor, enter another aquarium to feed on the crabs, and return to their own aquarium.[11]

The brain is protected in a cartilaginous cranium. The giant nerve fibers of the cephalopod mantle have been widely used for many years as experimental material in neurophysiology; their large diameter (due to lack of myelination) makes them relatively easy to study compared with other animals.[12]

Many cephalopods are social creatures; when isolated from their own kind, some species have been observed shoaling with fish.[13]

Some cephalopods are able to fly through the air for distances of up to 50 m. While cephalopods are not particularly aerodynamic, they achieve these impressive ranges by jet-propulsion; water continues to be expelled from the funnel while the organism is in the air.[14] The animals spread their fins and tentacles to form wings and actively control lift force with body posture.[15] One species, Todarodes pacificus, has been observed spreading tentacles in a flat fan shape with a mucus film between the individual tentacles[15][16] while another, Sepioteuthis sepioidea, has been observed putting the tentacles in a circular arrangement.[17]

Cephalopods have advanced vision, can detect gravity with statocysts, and have a variety of chemical sense organs.[7]^:34 Octopuses use their arms to explore their environment and can use them for depth perception.[7]

The primitive nautilus eye functions similarly to a pinhole camera.

Most cephalopods rely on vision to detect predators and prey, and to communicate with one another.[18] Consequently, cephalopod vision is acute: training experiments have shown that the common octopus can distinguish the brightness, size, shape, and horizontal or vertical orientation of objects. The morphological construction gives cephalopod eyes the same performance as sharks'; however, their construction differs, as cephalopods lack a cornea, and have an everted retina.[18] Cephalopods' eyes are also sensitive to the plane of polarization of light.[19] Unlike many other cephalopods, nautiluses do not have good vision; their eye structure is highly developed, but lacks a solid lens. They have a simple "pinhole" eye through which water can pass. Instead of vision, the animal is thought to use olfaction as the primary sense for foraging, as well as locating or identifying potential mates.

A cuttlefish with W-shaped pupils which may help them discriminate colors.

Surprisingly, given their ability to change color, all octopodes[20] and most cephalopods[21][22] are considered to be color blind. Coleoid cephalopods (octopus, squid, cuttlefish) have a single photoreceptor type and lack the ability to determine color by comparing detected photon intensity across multiple spectral channels. When camouflaging themselves, they use their chromatophores to change brightness and pattern according to the background they see, but their ability to match the specific color of a background may come from cells such as iridophores and leucophores that reflect light from the environment.[23] They also produce visual pigments throughout their body, and may sense light levels directly from their body.[24] Evidence of color vision has been found in the sparkling enope squid (Watasenia scintillans),[21][25] which achieves color vision by the use of three distinct retinal molecules: A1, most sensitive to green-blue (484 nm); A2, to blue-green (500 nm), and A4, to blue (470 nm), which bind to its opsin.[26]

In 2015, a novel mechanism for spectral discrimination in cephalopods was described. This relies on the exploitation of chromatic aberration (wavelength-dependence of focal length). Numerical modeling shows that chromatic aberration can yield useful chromatic information through the dependence of image acuity on accommodation. The unusual off-axis slit and annular pupil shapes in cephalopods enhance this ability.[27]

In 2015, molecular evidence was published indicating that cephalopod chromatophores are photosensitive; reverse transcription polymerase chain reactions (RT-PCR) revealed transcripts encoding rhodopsin and retinochrome within the retinas and skin of the longfin inshore squid (Doryteuthis pealeii), and the common cuttlefish (Sepia officinalis) and broadclub cuttlefish (Sepia latimanus). The authors claim this is the first evidence that cephalopod dermal tissues may possess the required combination of molecules to respond to light.[28]

Some squids have been shown to detect sound using their statocysts.[29]

This broadclub cuttlefish (Sepia latimanus) can change from camouflage tans and browns (top) to yellow with dark highlights (bottom) in less than a second.

Most cephalopods possess an assemblage of skin components that interact with light. These may include iridophores, leucophores, chromatophores and (in some species) photophores. Chromatophores are colored pigment cells that expand and contract in accordance to produce color and pattern which they can use in a startling array of fashions.[7][28] As well as providing camouflage with their background, some cephalopods bioluminesce, shining light downwards to disguise their shadows from any predators that may lurk below.[7] The bioluminescence is produced by bacterial symbionts; the host cephalopod is able to detect the light produced by these organisms.[30] Bioluminescence may also be used to entice prey, and some species use colorful displays to impress mates, startle predators, or even communicate with one another.[7]

Cephalopods can change their colors and patterns in milliseconds, whether for signalling (both within the species and for warning) or active camouflage,[7] as their chromatophores are expanded or contracted.[31] Although color changes appear to rely primarily on vision input, there is evidence that skin cells, specifically chromatophores, can detect light and adjust to light conditions independently of the eyes.[32] Cephalopods can use chromatophores like a muscle, which is why they can change their skin hue as rapidly as they do. Coloration is typically stronger in near-shore species than those living in the open ocean, whose functions tend to be restricted to disruptive camouflage.[7]^:2 Most octopuses mimic select structures in their field of view rather than becoming a composite color of their full background.[33]

Evidence of original coloration has been detected in cephalopod fossils dating as far back as the Silurian; these orthoconic individuals bore concentric stripes, which are thought to have served as camouflage.[34] Devonian cephalopods bear more complex color patterns, of unknown function.[35]

With the exception of the Nautilidae and the species of octopus belonging to the suborder Cirrina,[36] all known cephalopods have an ink sac, which can be used to expel a cloud of dark ink to confuse predators.[20] This sac is a muscular bag which originated as an extension of the hindgut. It lies beneath the gut and opens into the anus, into which its contents – almost pure melanin – can be squirted; its proximity to the base of the funnel means the ink can be distributed by ejected water as the cephalopod uses its jet propulsion.[20] The ejected cloud of melanin is usually mixed, upon expulsion, with mucus, produced elsewhere in the mantle, and therefore forms a thick cloud, resulting in visual (and possibly chemosensory) impairment of the predator, like a smokescreen. However, a more sophisticated behavior has been observed, in which the cephalopod releases a cloud, with a greater mucus content, that approximately resembles the cephalopod that released it (this decoy is referred to as a Pseudomorph). This strategy often results in the predator attacking the pseudomorph, rather than its rapidly departing prey.[20] For more information, see Inking behaviors.

The ink sac of cephalopods has led to a common name of "inkfish",[37] formerly the pen-and-ink fish.[38]

Viscera of Chtenopteryx sicula

Viscera of Ocythoe tuberculata

Cephalopods are the only mollusks with a closed circulatory system. Coleoids have two gill hearts (also known as branchial hearts) that move blood through the capillaries of the gills. A single systemic heart then pumps the oxygenated blood through the rest of the body.[39]

Like most molluscs, cephalopods use hemocyanin, a copper-containing protein, rather than hemoglobin, to transport oxygen. As a result, their blood is colorless when deoxygenated and turns blue when exposed to air.[40]

Cephalopods exchange gases with the seawater by forcing water through their gills, which are attached to the roof of the organism.[41]^:488[42] Water enters the mantle cavity on the outside of the gills, and the entrance of the mantle cavity closes. When the mantle contracts, water is forced through the gills, which lie between the mantle cavity and the funnel. The water's expulsion through the funnel can be used to power jet propulsion. The gills, which are much more efficient than those of other mollusks, are attached to the ventral surface of the mantle cavity.[42] There is a trade-off with gill size regarding lifestyle. To achieve fast speeds, gills need to be small – water will be passed through them quickly when energy is needed, compensating for their small size. However, organisms which spend most of their time moving slowly along the bottom do not naturally pass much water through their cavity for locomotion; thus they have larger gills, along with complex systems to ensure that water is constantly washing through their gills, even when the organism is stationary.[41] The water flow is controlled by contractions of the radial and circular mantle cavity muscles.[43]

The gills of cephalopods are supported by a skeleton of robust fibrous proteins; the lack of mucopolysaccharides distinguishes this matrix from cartilage.[44][45] The gills are also thought to be involved in excretion, with NH₄⁺ being swapped with K⁺ from the seawater.[42]

Octopuses swim headfirst, with arms trailing behind

While most cephalopods can move by jet propulsion, this is a very energy-consuming way to travel compared to the tail propulsion used by fish.[46] The efficiency of a propellor-driven waterjet (i.e. Froude efficiency) is greater than a rocket.[47] The relative efficiency of jet propulsion decreases further as animal size increases; paralarvae are far more efficient than juvenile and adult individuals.[48] Since the Paleozoic era, as competition with fish produced an environment where efficient motion was crucial to survival, jet propulsion has taken a back role, with fins and tentacles used to maintain a steady velocity.[4] Whilst jet propulsion is never the sole mode of locomotion,[4]^:208 the stop-start motion provided by the jets continues to be useful for providing bursts of high speed – not least when capturing prey or avoiding predators.[4] Indeed, it makes cephalopods the fastest marine invertebrates,[7]^:Preface and they can out-accelerate most fish.[41] The jet is supplemented with fin motion; in the squid, the fins flap each time that a jet is released, amplifying the thrust; they are then extended between jets (presumably to avoid sinking).[48] Oxygenated water is taken into the mantle cavity to the gills and through muscular contraction of this cavity, the spent water is expelled through the hyponome, created by a fold in the mantle. The size difference between the posterior and anterior ends of this organ control the speed of the jet the organism can produce.[49] The velocity of the organism can be accurately predicted for a given mass and morphology of animal.[50] Motion of the cephalopods is usually backward as water is forced out anteriorly through the hyponome, but direction can be controlled somewhat by pointing it in different directions.[51] Some cephalopods accompany this expulsion of water with a gunshot-like popping noise, thought to function to frighten away potential predators.[52]

Cephalopods employ a similar method of propulsion despite their increasing size (as they grow) changing the dynamics of the water in which they find themselves. Thus their paralarvae do not extensively use their fins (which are less efficient at low Reynolds numbers) and primarily use their jets to propel themselves upwards, whereas large adult cephalopods tend to swim less efficiently and with more reliance on their fins.[48]

Nautilus belauensis seen from the front, showing the opening of the hyponome

Early cephalopods are thought to have produced jets by drawing their body into their shells, as Nautilus does today.[53] Nautilus is also capable of creating a jet by undulations of its funnel; this slower flow of water is more suited to the extraction of oxygen from the water.[53] The jet velocity in Nautilus is much slower than in coleoids, but less musculature and energy is involved in its production.[54] Jet thrust in cephalopods is controlled primarily by the maximum diameter of the funnel orifice (or, perhaps, the average diameter of the funnel)[55]^:440 and the diameter of the mantle cavity.[56] Changes in the size of the orifice are used most at intermediate velocities.[55] The absolute velocity achieved is limited by the cephalopod's requirement to inhale water for expulsion; this intake limits the maximum velocity to eight body-lengths per second, a speed which most cephalopods can attain after two funnel-blows.[55] Water refills the cavity by entering not only through the orifices, but also through the funnel.[55] Squid can expel up to 94% of the fluid within their cavity in a single jet thrust.[47] To accommodate the rapid changes in water intake and expulsion, the orifices are highly flexible and can change their size by a factor of twenty; the funnel radius, conversely, changes only by a factor of around 1.5.[55]

Some octopus species are also able to walk along the seabed. Squids and cuttlefish can move short distances in any direction by rippling of a flap of muscle around the mantle.

While most cephalopods float (i.e. are neutrally buoyant or nearly so; in fact most cephalopods are about 2–3% denser than seawater[13]), they achieve this in different ways.[46] Some, such as Nautilus, allow gas to diffuse into the gap between the mantle and the shell; others allow purer water to ooze from their kidneys, forcing out denser salt water from the body cavity;[46] others, like some fish, accumulate oils in the liver;[46] and some octopuses have a gelatinous body with lighter chlorine ions replacing sulfate in the body chemistry.[46]

The Macrotritopus defilippi, or the sand-dwelling octopus, was seen mimicking both the coloration and the swimming movements of the sand-dwelling flounder Bothus lunatus to avoid predators. The octopuses were able to flatten their bodies and put their arms back to appear the same as the flounders as well as move with the same speed and movements.[57]

Females of two species, Ocythoe tuberculata and Haliphron atlanticus, have evolved a true swim bladder.[58]

Cross section of Spirula spirula, showing the position of the shell inside the mantle

Cuttlebone of Sepia officinalis

Gladius of Sepioteuthis lessoniana

Nautiluses are the only extant cephalopods with a true external shell. However, all molluscan shells are formed from the ectoderm (outer layer of the embryo); in cuttlefish (Sepia spp.), for example, an invagination of the ectoderm forms during the embryonic period, resulting in a shell (cuttlebone) that is internal in the adult.[59] The same is true of the chitinous gladius of squid[59] and octopuses.[60] Cirrate octopods have arch-shaped cartilaginous fin supports,[61] which are sometimes referred to as a "shell vestige" or "gladius".[62] The Incirrina have either a pair of rod-shaped stylets or no vestige of an internal shell,[63] and some squid also lack a gladius.[64] The shelled coleoids do not form a clade or even a paraphyletic group.[65] The Spirula shell begins as an organic structure, and is then very rapidly mineralized.[66] Shells that are "lost" may be lost by resorption of the calcium carbonate component.[67]

Females of the octopus genus Argonauta secrete a specialized paper-thin egg case in which they reside, and this is popularly regarded as a "shell", although it is not attached to the body of the animal and has a separate evolutionary origin.

The largest group of shelled cephalopods, the ammonites, are extinct, but their shells are very common as fossils.

The deposition of carbonate, leading to a mineralized shell, appears to be related to the acidity of the organic shell matrix (see Mollusc shell); shell-forming cephalopods have an acidic matrix, whereas the gladius of squid has a basic matrix.[68] The basic arrangement of the cephalopod outer wall is: an outer (spherulitic) prismatic layer, a laminar (nacreous) layer and an inner prismatic layer. The thickness of every layer depends on the taxa.[69] In modern cephalopods, the Ca carbonate is aragonite. As for other mollusc shells or coral skeletons, the smallest visible units are irregular rounded granules.[70]

Left: A giant squid found in Logy Bay, Newfoundland, in 1873. The two long feeding tentacles are visible on the extreme left and right.
Right: Detail of the tentacular club of Abraliopsis morisi

Cephalopods, as the name implies, have muscular appendages extending from their heads and surrounding their mouths. These are used in feeding, mobility, and even reproduction. In coleoids they number eight or ten. Decapods such as cuttlefish and squid have five pairs. The longer two, termed tentacles, are actively involved in capturing prey;[1]^:225 they can lengthen rapidly (in as little as 15 milliseconds[1]^:225). In giant squid they may reach a length of 8 metres. They may terminate in a broadened, sucker-coated club.[1]^:225 The shorter four pairs are termed arms, and are involved in holding and manipulating the captured organism.[1]^:225 They too have suckers, on the side closest to the mouth; these help to hold onto the prey.[1]^:226 Octopods only have four pairs of sucker-coated arms, as the name suggests, though developmental abnormalities can modify the number of arms expressed.[71]

The tentacle consists of a thick central nerve cord (which must be thick to allow each sucker to be controlled independently)[72] surrounded by circular and radial muscles. Because the volume of the tentacle remains constant, contracting the circular muscles decreases the radius and permits the rapid increase in length. Typically a 70% lengthening is achieved by decreasing the width by 23%.[1]^:227 The shorter arms lack this capability.

The size of the tentacle is related to the size of the buccal cavity; larger, stronger tentacles can hold prey as small bites are taken from it; with more numerous, smaller tentacles, prey is swallowed whole, so the mouth cavity must be larger.[73]

Externally shelled nautilids (Nautilus and Allonautilus) have on the order of 90 finger-like appendages, termed tentacles, which lack suckers but are sticky instead, and are partly retractable.

The two-part beak of the giant squid, Architeuthis sp.

All living cephalopods have a two-part beak;[7]^:7 most have a radula, although it is reduced in most octopus and absent altogether in Spirula.[7]^:7[74]^:110 They feed by capturing prey with their tentacles, drawing it into their mouth and taking bites from it.[20] They have a mixture of toxic digestive juices, some of which are manufactured by symbiotic algae, which they eject from their salivary glands onto their captured prey held in their mouths. These juices separate the flesh of their prey from the bone or shell.[20] The salivary gland has a small tooth at its end which can be poked into an organism to digest it from within.[20]

The digestive gland itself is rather short.[20] It has four elements, with food passing through the crop, stomach and caecum before entering the intestine. Most digestion, as well as the absorption of nutrients, occurs in the digestive gland, sometimes called the liver. Nutrients and waste materials are exchanged between the gut and the digestive gland through a pair of connections linking the gland to the junction of the stomach and caecum.[20] Cells in the digestive gland directly release pigmented excretory chemicals into the lumen of the gut, which are then bound with mucus passed through the anus as long dark strings, ejected with the aid of exhaled water from the funnel.[20] Cephalopods tend to concentrate ingested heavy metals in their body tissue.[75]

Amphioctopus marginatus eating a crab

The cephalopod radula consists of multiple symmetrical rows of up to nine teeth[76] – thirteen in fossil classes.[77] The organ is reduced or even vestigial in certain octopus species and is absent in Spirula.[77] The teeth may be homodont (i.e. similar in form across a row), heterodont (otherwise), or ctenodont (comb-like).[77] Their height, width and number of cusps is variable between species.[77] The pattern of teeth repeats, but each row may not be identical to the last; in the octopus, for instance, the sequence repeats every five rows.[77]^:79

Cephalopod radulae are known from fossil deposits dating back to the Ordovician.[78] They are usually preserved within the cephalopod's body chamber, commonly in conjunction with the mandibles; but this need not always be the case;[79] many radulae are preserved in a range of settings in the Mason Creek.[80] Radulae are usually difficult to detect, even when they are preserved in fossils, as the rock must weather and crack in exactly the right fashion to expose them; for instance, radulae have only been found in nine of the 43 ammonite genera,[81] and they are rarer still in non-ammonoid forms: only three pre-Mesozoic species possess one.[78]

Most cephalopods possess a single pair of large nephridia. Filtered nitrogenous waste is produced in the pericardial cavity of the branchial hearts, each of which is connected to a nephridium by a narrow canal. The canal delivers the excreta to a bladder-like renal sac, and also resorbs excess water from the filtrate. Several outgrowths of the lateral vena cava project into the renal sac, continuously inflating and deflating as the branchial hearts beat. This action helps to pump the secreted waste into the sacs, to be released into the mantle cavity through a pore.[82]

Nautilus, unusually, possesses four nephridia, none of which are connected to the pericardial cavities.

The incorporation of ammonia is important for shell formation in terrestrial molluscs and other non-molluscan lineages.[83] Because protein (i.e. flesh) is a major constituent of the cephalopod diet, large amounts of ammonium ions are produced as waste. The main organs involved with the release of this excess ammonium are the gills.[84] The rate of release is lowest in the shelled cephalopods Nautilus and Sepia as a result of their using nitrogen to fill their shells with gas to increase buoyancy.[84] Other cephalopods use ammonium in a similar way, storing the ions (as ammonium chloride) to reduce their overall density and increase buoyancy.[84]

Female Argonauta argo with eggcase and eggs

Detail of the hectocotylus of Ocythoe tuberculata

A dissected male specimen of Onykia ingens, showing a non-erect penis (the white tubular structure located below most of the other organs)

A specimen of the same species exhibiting an elongation of the penis to 67 cm in length

Cephalopods are a diverse group of species, but share common life history traits, for example, they have a rapid growth rate and short life spans.[85] Stearns (1992) suggested that in order to produce the largest possible number of viable offspring, spawning events depend on the ecological environmental factors of the organism. The majority of cephalopods do not provide parental care to their offspring, except, for example, octopus, which helps this organism increase the survival rate of their offspring.[85] Marine species' life cycles are affected by various environmental conditions.[86] The development of a cephalopod embryo can be greatly affected by temperature, oxygen saturation, pollution, light intensity, and salinity.[85] These factors are important to the rate of embryonic development and the success of hatching of the embryos. Food availability also plays an important role in the reproductive cycle of cephalopods. A limitation of food influences the timing of spawning along with their function and growth.[86] Spawning time and spawning vary among marine species; it's correlated with temperature, though cephalopods in shallow water spawn in cold months so that the offspring would hatch at warmer temperatures. Breeding can last from several days to a month.[85]

Cephalopods that are sexually mature and of adult size begin spawning and reproducing. After the transfer of genetic material to the following generation, the adult cephalopods then die.[85] Sexual maturation in male and female cephalopods can be observed internally by the enlargement of gonads and accessory glands.[87] Mating would be a poor indicator of sexual maturation in females; they can receive sperm when not fully reproductively mature and store them until they are ready to fertilize the eggs.[86] Males are more aggressive in their pre-mating competition when in the presence of immature females than when competing for a sexually mature female.[88] Most cephalopod males develop a hectocotylus, an arm tip which is capable of transferring their spermatozoa into the female mantel cavity. Though not all species use a hectocotylus; for example, the adult nautilus releases a spadix.[89] An indication of sexual maturity of females is the development of brachial photophores to attract mates.[90]

Cephalopods are not broadcast spawners. During the process of fertilization, the females use sperm provided by the male via external fertilization. Internal fertilization is seen only in octopodes.[87] The initiation of copulation begins when the male catches a female and wraps his arm around her, either in a "male to female neck" position or mouth to mouth position, depending on the species. The males then initiate the process of fertilization by contracting their mantle several times to release the spermatozoa.[91] Cephalopods often mate several times, which influences males to mate longer with females that have previously, nearly tripling the number of contractions of the mantle.[91] To ensure the fertilization of the eggs, female cephalopods release a sperm-attracting peptide through the gelatinous layers of the egg to direct the spermatozoa. Female cephalopods lay eggs in clutches; each egg is composed of a protective coat to ensure the safety of the developing embryo when released into the water column. Reproductive strategies differ between cephalopod species. In giant Pacific octopus, large eggs are laid in a den; it will often take several days to lay all of them.[87] Once the eggs are released and attached to a sheltered substrate, the females then die,[87] making them semelparous. In some species of cephalopods, egg clutches are anchored to substrates by a mucilaginous adhesive substance. These eggs are swelled with perivitelline fluid (PVF), a hypertonic fluid that prevents premature hatching.[92] Fertilized egg clusters are neutrally buoyant depending on the depth that they were laid, but can also be found in substrates such as sand, a matrix of corals, or seaweed.[86] Because these species do not provide parental care for their offspring, egg capsules can be injected with ink by the female in order to camouflage the embryos from predators.[86]

Most cephalopods engage in aggressive sex: a protein in the male capsule sheath stimulates this behavior. They also engage in male–male aggression, where larger males tend to win the interactions.[85] When a female is near, the males charge one another continuously and flail their arms. If neither male backs away, the arms extend to the back, exposing the mouth, followed by the biting of arm tips.[93] During mate competition males also participate in a technique called flushing. This technique is used by the second male attempting to mate with a female. Flushing removes spermatophores in the buccal cavity that was placed there by the first mate by forcing water into the cavity.[85] Another behavior that males engage in is sneaker mating or mimicry – smaller males adjust their behavior to that of a female in order to reduce aggression. By using this technique, they are able to fertilize the eggs while the larger male is distracted by a different male.[93] During this process, the sneaker males quickly insert drop-like sperm into the seminal receptacle.[94]

Mate choice is seen in cuttlefish species, where females prefer some males over others, though characteristics of the preferred males are unknown.[85] A hypothesis states that females reject males by olfactory cues rather than visual cues.[85] Several cephalopod species are polyandrous- accepting and storing multiple male spermatophores, which has been identified by DNA fingerprinting.[91] Females are no longer receptive to mating attempts when holding their eggs in their arms. Females can store sperm in two places (1) the buccal cavity where recently mated males place their spermatophores, and (2) the internal sperm-storage receptacles where sperm packages from previous males are stored.[85] Spermatophore storage results in sperm competition; which states that the female controls which mate fertilizes the eggs. In order to reduce this sort of competition, males develop agonistic behaviors like mate guarding and flushing.[85] The Hapalochlaena lunulata, or the blue-ringed octopus, readily mates with both males and females.[95]

In a variety of marine organisms, it is seen that females are larger in size compared to the males in some closely related species. In some lineages, such as the blanket octopus, males become structurally smaller and smaller resembling a term, "dwarfism" dwarf males usually occurs at low densities.[96] The blanket octopus male is an example of sexual-evolutionary dwarfism; females grow 10,000 to 40,000 times larger than the males and the sex ratio between males and females can be distinguished right after hatching of the eggs.[96]

Egg cases laid by a female squid

Cephalopod eggs span a large range of sizes, from 1 to 30 mm in diameter.[97] The fertilised ovum initially divides to produce a disc of germinal cells at one pole, with the yolk remaining at the opposite pole. The germinal disc grows to envelop and eventually absorb the yolk, forming the embryo. The tentacles and arms first appear at the hind part of the body, where the foot would be in other molluscs, and only later migrate towards the head.[82][98]

The funnel of cephalopods develops on the top of their head, whereas the mouth develops on the opposite surface.[99]^:86 The early embryological stages are reminiscent of ancestral gastropods and extant Monoplacophora.[98]

The shells develop from the ectoderm as an organic framework which is subsequently mineralized.[59] In Sepia, which has an internal shell, the ectoderm forms an invagination whose pore is sealed off before this organic framework is deposited.[59]

Chtenopteryx sicula paralarvae. Left: Two very young paralarvae. The circular tentacular clubs bear approximately 20 irregularly arranged suckers. Two chromatophores are present on each side of the mantle. Centre: Ventral, dorsal and side views of a more advanced paralarva. An equatorial circulet of seven large yellow-brown chromatophores is present on the mantle. Posteriorly the expanded vanes of the gladius are visible in the dorsal view. Right: Ventral and dorsal views of a very advanced paralarva.

Left: Immature specimens of Chiroteuthis veranyi. In this paralarval form, known as the doratopsis stage, the pen is longer than the mantle and 'neck' combined
Right: A mature Chiroteuthis veranyi. This species has some of the longest tentacles in proportion to its size of any known cephalopod.

The length of time before hatching is highly variable; smaller eggs in warmer waters are the fastest to hatch, and newborns can emerge after as little as a few days. Larger eggs in colder waters can develop for over a year before hatching.[97]

The process from spawning to hatching follows a similar trajectory in all species, the main variable being the amount of yolk available to the young and when it is absorbed by the embryo.[97]

Unlike most other mollusks, cephalopods do not have a morphologically distinct larval stage. Instead, the juveniles are known as paralarvae. They quickly learn how to hunt, using encounters with prey to refine their strategies.[97]

Growth in juveniles is usually allometric, whilst adult growth is isometric.[100]

The sequencing of a full Cephalopod genome has remained challenging to researchers due to the length and repetition of their DNA.[116] The characteristics of Cephalopod genomes were initially hypothesized to be the result of entire genome duplications. Following the full sequencing of a California two-spot octopus, the genome showed similar patterns to other marine invertebrates with significant additions to the genome assumed to be unique to Cephalopods. No evidence of full genome duplication was found.[117]

Within the California two-spot octopus genome there are substantial replications of two gene families. Significantly, the expanded gene families were only previously known to exhibit replicative behaviour within vertebrates.[117] The first gene family was identified as the Protocadherins which are attributed to neuron development. Protocadherins function as cell adhesion molecules, essential for synaptic specificity. The mechanism for Protocadherin gene family replication in vertebrates is attributed to complex splicing, or cutting and pasting, from a locus. Following the sequencing of the California two-spot octopus, researchers found that the Prorocadherin gene family in Cephalopods has expanded in the genome due to tandem gene duplication. The different replication mechanisms for Protocadherin genes indicate an independent evolution of Protocadherin gene expansion in vertebrates and invertebrates.[117]  Analysis of individual Cephalopod Protocadherin genes indicate independent evolution between species of Cephalopod. A species of shore squid Doryteuthis pealeii with expanded Protocadherin gene families differ significantly from those of the California two-spot octopus suggesting gene expansion did not occur before speciation within Cephalopods. Despite different mechanisms for gene expansion, the two-spot octopus Protocadherin genes were more similar to vertebrates than squid, suggesting a convergent evolution mechanism. The second gene family known as C2H2 are small proteins that function as zinc transcription factors. C2H2 are understood to moderate DNA, RNA and protein functions within the cell.[116]

The sequenced California two spot octopus genome also showed a significant presence of transposable elements as well as transposon expression. Although the role of transposable elements in marine vertebrates is still relatively unknown, significant expression of transposons in nervous system tissues have been observed.[118]  In a study conducted on vertebrates, the expression of transposons during development in Drosophila melanogaster activated genomic diversity between neurons.[119]  This diversity has been linked to increased memory and learning in mammals. The connection between transposons and increased neuron capability may provide insight into the observed intelligence, memory and function of Cephalopods.[118]

The approximate consensus of extant cephalopod phylogeny, after Strugnell et al. 2007, is shown in the cladogram.[65] Mineralized taxa are in bold. The attachment of the clade including Sepia and Spirula is unclear; either of the points marked with an asterisk may represent the root of this clade.

The internal phylogeny of the cephalopods is difficult to constrain; many molecular techniques have been adopted, but the results produced are conflicting.[65][120] Nautilus tends to be considered an outgroup, with Vampyroteuthis forming an outgroup to other squid; however in one analysis the nautiloids, octopus and teuthids plot as a polytomy.[65] Some molecular phylogenies do not recover the mineralized coleoids (Spirula, Sepia, and Metasepia) as a clade; however, others do recover this more parsimonious-seeming clade, with Spirula as a sister group to Sepia and Metasepia in a clade that had probably diverged before the end of the Triassic.[121][122]

Molecular estimates for clade divergence vary. One 'statistically robust' estimate has Nautilus diverging from Octopus at 415 ± 24 million years ago.[123]

Chambered nautilus (Nautilus pompilius)

Common cuttlefish (Sepia officinalis)

Atlantic bobtail (Sepiola atlantica)

European squid (Loligo vulgaris)

Common octopus (Octopus vulgaris)

The classification presented here, for recent cephalopods, follows largely from Current Classification of Recent Cephalopoda (May 2001), for fossil cephalopods takes from Arkell et al. 1957, Teichert and Moore 1964, Teichert 1988, and others. The three subclasses are traditional, corresponding to the three orders of cephalopods recognized by Bather.[124]

Class Cephalopoda († indicates extinct groups)

• Subclass Nautiloidea: Fundamental ectocochliate cephalopods that provided the source for the Ammonoidea and Coleoidea.
  • Order † Plectronocerida: the ancestral cephalopods from the Cambrian Period
  • Order † Ellesmerocerida (500 to 470 Ma)
  • Order † Endocerida (485 to 430 Ma)
  • Order † Actinocerida (480 to 312 Ma)
  • Order † Discosorida (482 to 392 Ma)
  • Order † Pseudorthocerida (432 to 272 Ma)
  • Order † Tarphycerida (485 to 386 Ma)
  • Order † Oncocerida (478.5 to 324 Ma)
  • Order Nautilida (extant; 410.5 Ma to present)
  • Order † Orthocerida (482.5 to 211.5 Ma)
  • Order † Ascocerida (478 to 412 Ma)
  • Order † Bactritida (418.1 to 260.5 Ma)
• Subclass † Ammonoidea: Ammonites (479 to 66 Ma)
  • Order † Goniatitida (388.5 to 252 Ma)
  • Order † Ceratitida (254 to 200 Ma)
  • Order † Ammonitida (215 to 66 Ma)
• Subclass Coleoidea (410.0 Ma-Rec)
  • Cohort † Belemnoidea: Belemnites and kin
    • Genus † Jeletzkya
    • Order † Aulacocerida (265 to 183 Ma)
    • Order † Phragmoteuthida (189.6 to 183 Ma)
    • Order † Hematitida (339.4 to 318.1 Ma)
    • Order † Belemnitida (339.4 to 66 Ma)
    • Genus † Belemnoteuthis (189.6 to 183 Ma)
  • Cohort Neocoleoidea
    • Superorder Decapodiformes (also known as Decabrachia or Decembranchiata)
      • Order Spirulida: Ram's horn squid
      • Order Sepiida: cuttlefish
      • Order Sepiolida: pygmy, bobtail and bottletail squid
      • Order Teuthida: squid
    • Superorder Octopodiformes (also known as Vampyropoda)
      • Family † Trachyteuthididae
      • Order Vampyromorphida: Vampire squid
      • Order Octopoda: octopus
    • Superorder † Palaeoteuthomorpha
      • Order † Boletzkyida

Other classifications differ, primarily in how the various decapod orders are related, and whether they should be orders or families.

This is the older classification that combines those found in parts K and L of the Treatise on Invertebrate Paleontology, which forms the basis for and is retained in large part by classifications that have come later.

Nautiloids in general (Teichert and Moore, 1964) sequence as given.

Subclass † Endoceratoidea. Not used by Flower, e.g. Flower and Kummel 1950, interjocerids included in the Endocerida.

Order † Endocerida

Order † Intejocerida

Subclass † Actinoceratoidea Not used by Flower, ibid

Order † Actinocerida

Subclass Nautiloidea Nautiloidea in the restricted sense.

Order † Ellesmerocerida Plectronocerida subsequently split off as separate order.

Order † Orthocerida Includes orthocerids and pseudorthocerids

Order † Ascocerida

Order † Oncocerida

Order † Discosorida

Order † Tarphycerida

Order † Barrandeocerida A polyphyletic group now included in the Tarphycerida

Order Nautilida

Subclass † Bactritoidea

Order † Bactritida

Paleozoic Ammonoidea (Miller, Furnish and Schindewolf, 1957)

Suborder † Anarcestina

Suborder † Clymeniina

Suborder † Goniatitina

Suborder † Prolecanitina

Mesozoic Ammonoidea (Arkel et al., 1957)

Suborder † Ceratitina

Suborder † Phylloceratina

Suborder † Lytoceratina

Suborder † Ammonitina

Subsequent revisions include the establishment of three Upper Cambrian orders, the Plectronocerida, Protactinocerida, and Yanhecerida; separation of the pseudorthocerids as the Pseudorthocerida, and elevating orthoceratid as the Subclass Orthoceratoidea.

Shevyrev (2005) suggested a division into eight subclasses, mostly comprising the more diverse and numerous fossil forms,[125][126] although this classification has been criticized as arbitrary.[127]

Gyronaedyceras eryx, a nautiloid from the Devonian of Wisconsin

Various species of ammonites

Holotype of Ostenoteuthis siroi from family Ostenoteuthidae.

A fossilised belemnite

Class Cephalopoda

• Subclass † Ellesmeroceratoidea
  • Order † Plectronocerida (501 to 490 Ma)
  • Order † Protactinocerida
  • Order † Yanhecerida
  • Order † Ellesmerocerida (500 to 470 Ma)
• Subclass † Endoceratoidea (485 to 430 Ma)
  • Order † Endocerida (485 to 430 Ma)
  • Order † Intejocerida (485 to 480 Ma)
• Subclass † Actinoceratoidea
  • Order † Actinocerida (480 to 312 Ma)
• Subclass Nautiloidea (490.0 Ma- Rec)
  • Order † Basslerocerida (490 to 480 Ma)
  • Order † Tarphycerida (485 to 386 Ma)
  • Order † Lituitida (485 to 480 Ma)
  • Order † Discosorida (482 to 392 Ma)
  • Order † Oncocerida (478.5 to 324 Ma)
  • Order Nautilida (410.5 Ma-Rec)
• Subclass † Orthoceratoidea (482.5 to 211.5 Ma)
  • Order † Orthocerida (482.5 to 211.5 Ma)
  • Order † Ascocerida (478 to 412 Ma)
  • Order † Dissidocerida (479 to 457.5 Ma)
  • Order † Bajkalocerida
• Subclass † Bactritoidea (422 to 252 Ma)
• Subclass † Ammonoidea (410 to 66 Ma)
• Subclass Coleoidea (410.0 Ma-rec)[128]

Pyritized fossil of Vampyronassa rhodanica, a vampyromorphid from the Lower Callovian (166.1 million years ago)

Another recent system divides all cephalopods into two clades. One includes nautilus and most fossil nautiloids. The other clade (Neocephalopoda or Angusteradulata) is closer to modern coleoids, and includes belemnoids, ammonoids, and many orthocerid families. There are also stem group cephalopods of the traditional Ellesmerocerida that belong to neither clade.[129][130]

The coleoids, despite some doubts,[1]^:289 appear from molecular data to be monophyletic.[131]