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Lophotrochozoa : Mollusca

The Cephalopoda
Squids, octopuses, nautilus, and ammonites

FUN FACT: From the dark abyss to shallow tide pools, research has recently revealed some of the mysterious behaviors of two famed cephalopods, the Giant Squid and the deadly Blue-ringed octopus (click image below for an enlargement).

Blue-ringed octopus
Cephalopods are the most intelligent, most mobile, and the largest of all molluscs. Squid, octopuses, cuttlefish, the chambered nautilus, and their relatives display remarkable diversity in size and lifestyle with adaptations for predation, locomotion, disguise, and communication. These "brainy" invertebrates have evolved suckered tentacles, camera-like eyes, color-changing skin, and complex learning behavior. Their lengthy evolutionary history spans an impressive 500 million years and the abundant fossils they've left behind (mostly shelled nautiloids and ammonoids) record repeated speciation and extinction events. From myths about their enigmatic fossilized remains to fantastic accounts of tentacled sea monsters, cephalopods also figure prominently in the literature and folklore of human societies around the world. Today, biologists and paleontologists continue to captivate the human mind and imagination with details of these molluscs' behavior, natural history, and evolution.

Cephalopoda cladogram A
Fossil record
There are about 17,000 named species of fossil cephalopods, compared to the 800 identified living species of cephalopods. Clearly the lineages of extinct taxa were prolific and diverse. So diverse in fact, that paleontologists have identified three distinct fossil clades that are entirely extinct: Endoceratoidea, Actinoceratoidea, and Bactritoidea (cladogram A, at right). All members of these clades were squid-like, but had straight external shells called orthocones. They flourished in Paleozoic oceans between the Ordovician (488 mya) and Triassic periods (200 mya) with shells that, in some species, reached nearly 10 meters in length.

More familiar to us in the fossil record are the nautiloids, ammonoids, and belemnites.

Nautiloids and ammonoids
Nautiloids are the earliest cephalopods found in the fossil record, appearing by the Late Cambrian. The earliest forms were orthoconic (having straight shells), but during the Ordovician the nautiloids experienced a rapid diversification and evolved a planispiral (coiled in a single plane) shell shape. All have shells with nacre and interconnected internal chambers, similar to what we see in the modern nautilus. This morphology is very similar to many of the ammonoids, which first appear in coiled form in the Devonian Period. Though nautiloids and ammonoids may appear the same, they are easily distinguished by the location of their siphuncle and the shapes of their sutures.

Position of the siphuncle in ammonoids; two nautiloids with simple sutures
The photo on the left shows the position of the siphuncle in ammonoids. The other two are of nautiloids exhibiting the simple sutures typical of the group.

The siphuncle is an internal tube that runs through and connects the chambers of the shell. In nautiloids, it runs through the center of the shell chambers, while in almost all planispiral ammonoids, it is found along the shell's outer edge (above left). Sutures are contact lines between shell chamber walls (called septa) and the inner shell wall of nautiloid and ammonoid shells. In nautiloids these lines are straight and are called simple sutures (above center and right). In contrast, ammonoid sutures dip and fold in undulations called lobes and saddles (below left). The most undulated, complex sutures are found in the prolific ammonoids of the Cretaceous, the ammonites (below right). One pattern of change in the evolution of ammonoids as a clade is that their suture morphology became more complex with time. That is, ammonoids from the Cretaceous have sutures with more intricate lobes and saddles than those of their relatives from the Permian 200 million years earlier.

Ammonoids with more complex sutures
Hildoceras bifrons (left) illustrates the typical lobes and saddles of ammonoid sutures. The sutures on the ammonite (right) are even more complex.

FUN FACT: Ammonoids, like belemnites, have also played a notable role in folklore. During the Middle Ages, their coiled shells were interpreted by the English, who encountered them in Jurassic-aged rocks exposed throughout Great Britain, as lithified snakes (called "snake stones"). Similarly, ammonite fossils encountered by the early Romans were mistaken for horns, and termed "ammonites" for the coiled horns of the Egyptian ram-god Ammon.
Suture patterns and lifestyle: The diversity of this suture geometry has inspired paleontologists to investigate its function. In one study, paleontologists (Daniel et al. 1997) used modeling to determine if there was a relationship between the pattern of lobes and saddles and buoyancy and the ability to withstand pressure. They found that simple sutures, like those in nautiloids and early ammonoids, can withstand great pressure but have poor buoyancy control. They interpret that these animals lived at depth and were not fast moving. In contrast, complex sutures like those in ammonites of the Cretaceous did not withstand pressure well, but allowed for very effective buoyancy control. They infer that this reflects a lifestyle at shallower depths. Based on this evidence, it appears that many ammonoid lineages evolved over millions of years, beginning in deep water habitats and evolving to inhabit relatively shallow ones.

Shell morphology: Another characteristic unique to ammonoid cephalopods is that although most were planispiral, the shells of some species were wide, open-coiled, kinked, twisted, or hooked. The implications of these shapes on the animals' behavior and lifestyle could be profound, but how could it be tested? The answer is through inference. One way paleontologists infer function from an organism's shape or form, is through experimentation and comparison with living animals. In this case, paleontologists measured buoyancy and hydrodynamic characteristics of Nautilus, and compared their results to actual tests of ammonoid shells and models in a water flume. They found that planispiral shell shapes (like a discus) were able to move through the water quickly, while wider and more open shell shapes moved more slowly. These morphologies could mean that planispiral cephalopods lived an active, pelagic lifestyle and wider shelled ammonoids lived near the ocean bottom and were slow movers. Dramatic curves, twists, as well as highly ornate ammonoid shells also suggest that those animals were relatively slow movers inhabiting a quiet marine environment.

Belemnites

Belemnite fossils
The rostrum of belemnites is the part most frequently preserved (left). At right, a long belemnite rostrum in a block containing other marine fossils.
The fossil record of most cephalopods in the clade Coloidea (squid, cuttlefish, octopuses, and their relatives) is poor, especially when compared to their shelly relatives. Their hard parts, if any, are internal, can be greatly reduced in size, and often lack calcification. The extinct belemnites, however, are the exception. These squid-like animals (below) swam with ammonoids and nautiloids in oceans of the Triassic, Jurassic, and Cretaceous Periods and are considered by paleontologists to be the ancestors of the Coleoidea. Like orthocones, belemnites had a straight shell, but it was internal, not external. It was made of three parts, a proostracum and phragmocone followed by a rostrum. Being highly resistant, the posterior bullet-shaped rostrum is most often preserved and can be found in great quantity and concentration in Mesozoic marine sediments (see photos). Before these bullet-shaped fossils were understood as fossils, early Europeans explained them as the products of lightning hitting the ground and named them "thunderbolts" or "thunderstones."

Basic belemnite anatomy

Cephalopoda cladogram B
Despite the great diversity in size, shell morphology, behavior, and lifestyle, cephalopods are all united by a suite of shared molluscan characters. They are marine, predatory, and have at least eight arms derived from the molluscan foot. All have a modified radula, and a horny, parrot-like beak for subduing prey. Their mantle is modified into a siphon for movement via jet-propulsion, and their highly developed nervous and sensory systems include complex eyes and a centralized brain. Their name, Cephalopod or "head-foot" in Greek, reflects the unique relationship between the cephalopod head and foot: the arms encircle the animals' head.

Life history & ecology
Three main clades are typically identified within the Cephalopoda (cladogram B, left): the Ammonoidea (an extinct and shelled clade), Nautiloidea (with only one living shelled genus, Nautilus) and Coleoidea (squids, cuttlefish, octopuses, the Ram's Horn Squid, the "paper nautilus," and an extinct clade, the belemnites). The ammonoid lineage survived for 300 million years in the oceans of the Paleozoic and Mesozoic. Most had planispiral (coiled in a single plane) external shells, and throughout their evolutionary history these plentiful predators shared the seas with the nautiloids, a clade of less diverse shelled cephalopods. By the end of the Cretaceous Period however, extinction had wiped out the ammonoids entirely and left only one surviving nautiloid clade, the genus Nautilus. Today, the only living representatives of shelled cephalopods are a few species of Nautilus. These molluscs are slow-moving, restricted to deep water, and have coiled shells that are similar to those of their fossil ancestors.

Nautilus, Ram's Horn Squid, and Paper Nautilus
From left, the exterior shell of the extant Nautilus; a cross-section of the Nautilus shell; the internal shells of the Ram's Horn Squid (Spirula spirula); and the secreted external papery shell-like brood pouch of the female Paper Nautilus (Argonauta sp.).

Octopus
A female Octopus digueti.
Members of the Coleoidea are probably the best known of the Cephalopoda, as this group contains the squids (Teuthoidea) and octopuses (Octopoda) (right). Also included in this clade are the lesser-known cuttlefish (Sepioidea), the Ram's Horn Squid, which has an internal coiled shell and floats head down in the water, and an enigmatic deep water genus called the "vampire squid" (Vampyromorpha). The majority of coleoids are squid species, and most of these animals are torpedo-shaped, fast moving, and have a thin, flexible internal shell called a pen. Cuttlefish (sometimes called "cuttles") look like squid, but have stouter bodies with a broad internal shell called a cuttlebone or sepion. They move mostly by undulating their body fins and can live in the water column or at the sediment surface. Octopuses are adapted to a benthic lifestyle, have no shell, can mimic their surroundings, and even "walk" on two of their eight arms. Belemnites are sometimes considered the sister group of extant (living) coleoids, but have also been interpreted as their ancestor.

FUN FACT: In 2006, a UC Berkeley graduate student reported that the Indonesian Coconut Octopus, Octopus marginatus, can move along the ocean floor using only the tips of its arms, almost like "walking." See Crissy Huffard's "Walktopus."
Based on molecular and morphological data, the extant Coleoidea is a monophyletic group (cladogram C, below). It is the sister group of the living species of Nautilus, which is also a monophyletic clade, albeit of only a few species (D, below). The phylogenetic relationships within the coleoids is less clear. Some cladograms depict the Sepioidea (cuttlefish), Teuthoidea (squid), Vampyromorpha (vampire "squid"), and Octopoda (octopuses) as coupled into two sets of sister groups, the Decabrachia and Octopodiformes (E, below). While the cladograms from another study (Lindgren et al. 2004) illustrate that although the coleoids are monophyletic, the cuttlefish (Sepiodea) are nested within the squids (Teuthoidea), making the Teuthoidea clade paraphyletic (F, below right).

Cephalopoda cladograms C, D, and E

More on morphology

Cephalopoda cladogram F
The external shell. One of the most obvious differences in body type, which for cephalopods does reflect shared ancestry, is the presence or absence of an external shell. Clades without an external shell are called endocochleate and include the coleoids; squids, cuttlefish, and octopuses. The internal shell of these taxa, called a gladius, can be cartilaginous, calcareous, chitinous or absent entirely. Presence of an external shell, such as that of the Nautiloids, Ammonoids, and orthoconic cephalopods, is considered a plesiomorphic, or ancestral state.

The eye. No presentation of cephalopods would be complete without a discussion of the cephalopod eye. This structure is probably the most sophisticated eye of all invertebrates and is as complex as the vertebrate eye, though the two are not homologous. For their body size, cephalopod eyes are relatively large. They contain an iris, pupil, and lens, but not necessarily a cornea. Octopuses are the only cephalopods with a completely protected "closed" cornea. That means that the eyes of squids and sepioids (cuttlefish, etc.) are in direct contact with sea water! The pupil in cephalopods is unique in that its morphology is different in octopuses, cuttlefish, and squid. Octopuses have a slit-shaped rectangular pupil. In cuttlefish it is W-shaped, and in squid it is round (see below). In Nautilus the eye is much simpler. It is mounted on a stalk, has no lens, and has a very small pupil (1-2 mm). It can narrow and widen in different brightnesses but resolves images poorly, so probably is useful only to detect light.

Eye morphology in cephalopods
Differing eye morphologies in cephalopods. From left, a squid (Loligo), octopus, cuttlefish, and Nautilus. Note the hyponome below the octopus eye — this is a muscular tube, that when contracted, expels water in a jet, propelling the octopus backwards. The hyponome can be aimed in various directions, giving the octopus finer control over its escape route.

Arms and tentacles. Arms and tentacles are another distinguishing cephalopod characteristic. All cephalopods have arms, but not all cephalopods have tentacles. Octopuses, cuttlefish, and squid have eight non-retractable arms, but only cuttlefish and squid (Sepioidea and Teuthoidea) have tentacles (two each). Arms usually have cirri (fleshy papillae/palps), often suckers, and sometimes hooks (modified suckers) along their undersides. These can be attached to the arm directly or by a flexible stalk and are used to adhere to substrates and catch prey. Tentacles are longer than arms, are retractable, and usually have a blade-shaped or flattened tip, called a club, which is covered in suckers. Squid and cuttlefish have one pair of tentacles and they use these to strike quickly at prey.

FUN FACT: The largest cephalopod Mesonychoteuthis hamiltoni, (Fig. 17) called the colossal squid, is longer than a city bus, while the smallest cephalopod, Idiosepius notoides, the pygmy squid, could fit on your fingernail.
Sex and reproduction. Sex and reproduction in cephalopods is in many ways quite different than in other molluscs. First, sexes are separate and mating usually includes a courtship that often involves elaborate color changes. This is followed by the transfer of a spermatophore (sperm packet) by a male to a female through her mantle opening. The spermatophore is transferred by the male using either a penis or a modified arm called a hectocotylus. Most females then lay large yolky eggs in clusters on the ocean floor or on any other hard substrate. Eggs develop by dividing unequally instead of in the spiral pattern of other molluscs. It is thought this is a derived mode of development. After a period of development within the egg, juveniles hatch out directly without the swimming larval stage common to many other molluscs. Most males and females die shortly after spawning.

FUN FACT: A hectocotylus is a cephalopodic arm of a male, modified to deliver a spermatophore (sperm-containing sac) to a female. In some taxa, part of this arm can detach from the male and remain inside the female. In 1829, the famous naturalist George Cuvier first identified and described a hectocotylus in the paper nautilus (an octopus of the genus Argonauta) but, at the time he thought that this detached arm was a parasitic worm! He named it Hectocotylus octopodis. When it was discovered that the "worm" was really a cephalopod arm, the name "hectocotylus" was kept but its meaning changed to refer to the spermatophore-transferring arm of any male cephalopod.
Chromatophores on a baby blue-ring octopus
Chromatophores of Octopus bimaculoides
Top: The chromatophores on this three-millimeter-long, 12-hour-old baby blue-ring octopus are clearly visible. Bottom: Click on this photo to see an enlargement — you'll need to in order to see the chromatophores (the dark stippling) on the skin of this California Two-spot Octopus (Octopus bimaculoides).
Changing color. Cephalopods have an amazing ability to change color very rapidly. They accomplish this feat using numerous pigment-filled bags, called chromatophores. Chromatophores are found in the skin, and expand and contract to reveal or conceal small dots of color (left). They can be so densely concentrated that 200 may be found in a patch of skin the size of a pencil eraser! Additionally, an iridescent dermal tissue can also be manipulated by some cephalopods to aid in camouflage, courtship rituals, or accompany color changes.

Some pelagic squids possess an additional color-changing structure; the light organ. A pair of these light organs is located within the mantle cavity on the underside of the squid. Each contains a crypt and a lens. A crypt is a small sac that houses luminous bacteria and a lens is a complex stack of tiny reflecting plates that controls the luminescence of this bacteria. Light from the bacteria projects downward and the squid can manipulate its intensity to match any light coming from above. This masks the squid's own silhouette, protecting it from potential predators.

The brain. Finally, one of the most intriguing aspects of cephalopods is their intelligence. With a centralized brain, the largest of all invertebrates, and highly developed eyes and other sense organs, they are able to remember and learn by example or through trial and error.

References and resources

Web resources

Original text by Jann Vendetti, UCMP, 2006. Blue-ringed octopus (adult and baby) and Octopus digueti photos by Roy Caldwell, Integrative Biology and UCMP, UC Berkeley; ammonoid, nautiloid, belemnite, Nautilus shell, Ram's Horn Squid, and paper nautilus photos by Jann Vendetti, UCMP; cephalopod eye morphology and Octopus bimaculoides photos © Larry Jon Friesen.