A Land Octopus (Speculative Evolution)

This will be an exploration of hypothetical land cephalopods, followed by my own take on the trope.

For a great many people, the 2002 series, or the ensuing franchise, The Future is Wild was their first exposure to the scientific and literary fields of specevo (speculative evolution). While the franchise has been criticised for some of its more fanciful elements not grounded in any sort of biology, undoubtedly one of its most iconic creations were the terasquids.

A megasquid, a representative of the terasquids.

Pictured here is one terasquid, the megasquid. The megasquid is supposedly a descendent of squid. However, the jump from water to land would be more plausibly made by their more benthic dwelling cousins, the octopus. And indeed, the series did feature an amphibious octopus earlier on, the social fresh water swampus. Regardless, the megasquid is widely considered unrealistic.

Megasquid anatomy.

The legs of this elephant sized animal are canonically described as being composed entirely of muscle. The authors justified this with some back-of-the-envelope calculations, but in reality such a creature would likely crumple under its own weight if it were to try to stand and walk.

The maximum size an animal can achieve is largely dictated by the kind of skeleton it has. Skeletons can be broadly divided into one of three categories; hydrostatic, endo- and exo-.

Endoskeletons support the largest land animals that live and have ever lived to date. These are familiar animals such as the African elephant, which as the largest land animal alive today, weighing in at 6 tons. The largest size thought to have ever been achieved by a mammal was by indricotherium. A relative of modern day rhinoceroses, indricotherium could weigh an estimated 30 tons. The largest land animal of all time however was probably a titanosaur, with the largest weighing an estimated 70 tons. All of these animals were vertebrates possessing hard supportive endoskeletons.

Hydrostatic skeletons are perhaps the most simple. Muscular hydrostats are structures of radial and longitudinal muscle bands which work against their own incompressibility as leverage.

Elephant trunks and human tongues are both examples of muscular hydrostats. Animals that rely entirely on hydrostatic skeletons include slugs, jellyfish, octopus and earthworms. In water, a hydrostatic skeleton is not as much of a limiter on size as buoyancy supports much of the body weight. A colonial siphonophore (a cnidarian, like jellyfish) can grow as long as 50 metres, longer than a blue whale. The largest octopus, the giant Pacific octopus, can weigh up to 300 kilograms and have an arm span of 9 metres.

On land, the largest slug, the ash-black slug can be as long as 15 centimetres. And the largest earthworm in the world, the Giant Gippsland Earthworm can be up to 1.5 metres long and weigh as much as 400 grams. Impressive, but not nearly as much as the soft bodies of the ocean.

Exoskeletons provide more support but limit the growth of animals in other ways. The largest land animal with an exoskeleton is the coconut crab, an enormous hermit crab relative that is 1 metre across and weighs about 4.5 kilograms.

While impressive, these land invertebrates are minuscule by comparison even to ourselves.

It's hard imagine them contending with elephants.

The swampus. An amphibious social freshwater swamp octopus.

The swampus was perhaps a better depiction of a land cephalopod than the megasquid, flat and squishy, somewhat clumsy on land, capable of short bursts of moderate speed at best. As with any work of speculative fiction, we can't really know if such a thing could ever be. But for the swampus to evolve a number of things would have to happen.

The swampus is said to be a freshwater cephalopod. There are no known living or extinct examples of freshwater cephalopods. It could be because these niches are just too crowded for cephalopods to make the costly evolutionary leap to fresh water. Although some octopus can tolerate brackish water, the ion pumps of the cephalopod nephridia (their equivalent of kidneys) must work to keep salt out of the body. Going into fresh water, they would need to flip to keep salt in the body. That being said, this is not an insurmountable leap and anadromous fish like salmon even make the transition within the same lifetime.

To go from aquatic to amphibious, an animal needs to be able to absorb oxygen from air. Gills are excellent for breathing underwater but dry up in air. Their large surface area is what allows them to efficiently absorb oxygen. But moving into air removes the water that usually separates the delicate folds of tissue, causing them to collapse and losing that vital surface area. Many of the octopus's molluscan cousins within the class gastropoda have already evolved to breathe air. These terrestrial pulmonate slugs and snails have lost their gills altogether and instead have converted the highly vascularised walls of their mantel cavity into a "pallial lung". A simple vascularised wall may be insufficient for the relatively active life of a cephalopod. Vertebrate amphibians avoid this same problem by having low metabolisms and breathing partly through their skin. Consistent with this, the swampus stores up oxygen in its tissues and must return to water occasionally to replenish it.

And like the vertebrate amphibians, the swampus is still tied to water for reproduction. The eggs of amphibians and octopuses are without a shell and their young are unable to survive out of water for long. The amniote vertebrates long ago solved this problem by laying hard shelled eggs that hold moisture in.

The swampus also uses four of its arms as feet, much like a snails. Although even in their current form, some octopuses are not known to be shy about moving on land.

Having such a versatile body and inhabiting coastal waters occasionally drives some species of octopus onto land to search for food or flee predators. Although this is far from true amphibiousness, with the octopuses needing to quickly return to water to breathe and survive.

Though with that out of the way and without further ado, I present my own hypothetical evolution of a land cephalopod.

The setting for this work of speculative evolution will focus mainly on the octopus itself and not so much on its predators, prey and environment.

It starts with a normal octopus body plan.

Stage 1: A normal octopus with beak, stylets and mantle cavity highlighted. Within the mantle cavity is the siphon, gills and an oviduct.

Octopus are remarkable animals as is; eight arms, three hearts, no bones, a beak, blue blood, neurotoxic venom, camouflage skin, and a brain bigger than something related to a clam has any business having, in the shape of a doughnut.

The eight arms of the octopus surround its beaked mouth and are derived from the molluscan foot, the same tissue that makes the fleshy pad slugs and snails slide around on. These eight limbs each contain a central nerve cord leading to a ganglion, a knot of nerves that makes decisions for each arm, then from each ganglion on to the central brain, which is itself is wrapped around the oesophagus. Each arm can move independently, taste, touch and grab using muscular suction cups.

The "head" of the octopus actually occurs in the middle of its body. Above the head is the visceral hump where the organs are kept. Like all molluscs, the octopus body is surrounded by a thick mantel, a layer of tissue that would have excreted a calcerous shell in their ancestors. The coleoid branch of the cephalopod tree however evolved to internalise this shell to swim faster. The only remnants of a shell in octopuses are two rods of cartilage adjacent to the visceral cavity known as stylets.

An octopus stylet. (Source: https://www.researchgate.net/profile/Stephen-Leporati/publication/277224563/figure/fig1/AS:365909345619968@1464250994449/An-Octopus-pallidus-stylet.png)

Also like other molluscs, the mantle includes a cavity with anus, gills, urinary tract and reproductive organs. Cephalopods also posses a siphon, a muscular tube which allows them to pump water uni-directionally over the gills, avoiding pumping deoxygenated water back over them, and allowing them to achieve their iconic jetting motion. Each of the two gills has its own brachial heart in addition to the single two chambered systemic heart. This in effect achieves something like the four chambered vertebrate heart using three separate hearts.

Octopuses are already capable of moving on land. The first adaptation for life on land could be considered more behavioural than physical.

Stage 2: No apparent physical adaptations.

The arms which the octopus usually uses to pull itself through the rocks of tidal pools and reefs can work just as well to pull it along sandy beaches and into the rock pools on the shore. From inspecting video, it appears they pull themselves forward in a sort of "horizontal dog-paddle" motion. These first steps would be motivated by the abundance of crabs fleeing predation from below the water.

As this behaviour becomes more advantageous by allowing octopuses to pursue prey that spends more time above water, the adaptation of wider more specialised "flippers" might be selected for. I'll call this octopus "platycnemis", or "flat shinned one".

Stage 2: An octopus with flippers.

These flippers would still allow mobility beneath water, but would be more useful on land than tentacles. They're somewhat modelled after the flippers of sea turtles and seals. The platycnemis would use them in a paddling motion to skip off of sand and rocks. To keep the flippers rigid, the radial muscles would need to be in constant action. Over time, the connective tissue matrix of those muscles might harden and allow the radial muscles to relax. This would leave a cartilaginous structure where the radial muscle was.

To help with movement on land and hold onto dry objects without the aide of suction, small chitinous spikes could emerge on the arms at the rim of suckers. These denticles are already present in squids. The inside surface of every cephalopod sucker is already coated by a thin cuticle of chitin to protect the muscle underneath. Squid have evolved these cuticles into sharp gripping hooks for snaring prey. The platycnemis could use the same denticles for mobility on land.

Long stylets would lend some stiffness to the body. There would be selective pressure for longer stiffer stylets. Having a rigid body would help the platycnemis move more efficiently.

These stylets may eventually even get long enough to act as a spring, storing kinetic energy between limb strokes.

To support this vigorous mode of transportation on land, the platycnemis carries a small volume of water around with it inside its mantle cavity. It uses its siphon to periodically pump bubbles of air past its gills, oxygenating the water and expelling carbon dioxide. The platycnemis still spends the majority of its time swimming underwater.

While the evolution of a pallial lung is feasible for the sedentary gastropods, cephalopods are more active. A pallial lung would bypass the brachial hearts, lowering respiratory efficiency. In the short term, the lung would also be less vascularised than gills. While cephalopods do have the advantage over gastropods of oxygen carrying haemocyanin based blood, it is not nearly as effective as vertebrate haemoglobin blood at ambient temperatures and pressure. None of these challenges are insurmountable for natural selection but the exaptation of the gills would perhaps be the most direct path for such an organism as the octopus with it's many oxygen-hungry neurons. The common octopus has more neurons than even some mammals and can't afford to lose that oxygen absorption capacity.

The platycnemis hunts crabs. It chases its prey first in water, then it pursues them onto land, using its flippers to skip after the crabs before grabbing them with its hooked front arms. The pupils of the octopus have become narrower to assist in its new style of pursuit and better watch the skies above for areal predators. When threatened, it will flash black and white warning colours and lift its hooked arms to show off its venomous beak. The eggs of the platycnemis are still laid in water and their young grow up much like any octopus until they are mature.

I will dub the next step in this hypothetical evolution the "ambulopus" for "walking octopus" as our creation takes its first real steps on land.

Stage 3: A stumpy four legged octopus.

The continued stiffening of the radial muscles into cartilage has given rise to stiff "bones". These bones give just enough stiffness to the four stubby walking limbs that they can just barely hold the ambulopus above the ground while sprawled out to the side. The sharp chitin denticles of the platycnemis have folded up and blunted out to form protective "tonenails" for the ambulopus to walk on.

The hump has undergone rotation to bring the legs beneath the animal. The mantle cavity has likewise rotated so that it now sits at the end of the ambulopus. The beak however has stayed in its position at the front of the animal rather than staying at the centre of the molluscan "foot", which is now spread out beneath the animal. This is because the octopus's oesophagus travels through the lobes of the brain, to which the eyes are attached. The mouth must therefore stay at the front with the eyes.

The stylets have further lengthened to bare some of the weight of the body as the ambulopus lifts its hump above the ground. The alternating bending and flexing of each stylet allows the ambulopus to run for brief periods, evading predators and chasing down livelier prey than before.

The ambulopus does not carry a mantle cavity full of water as the platycnemis does. Instead, the ambulopus's gills have evolved a rigid frame and natural surfactants to help keep the delicate folds of vascular tissue open when exposed to air. The siphon acts as a moist surface to keep the air inside the mantle cavity from drying out the gills completely.

Its pupils have further rounded as it begins to stand above the flat horizon. The support of solid limbs has allowed it to grow a heavier gut and become more herbivorous. The ambulopus will run and attempt to camouflage as a large rock when threatened. Reproduction is still tied to the water, but the ambulopus is beginning to birth fewer and larger eggs which hatch into more well developed offspring. These offspring will thus spend less of its life competing with other octopuses in the water and more time on land, where it is better suited to life. This animal spends as much time under water as above it. The ambulopus is truly amphibious.

The final step evolution of the land cephalopod, I will call "styloctopus", or "upright octopus".

Stage 4: A fully terrestrial octopus; the styloctopus

The chitinous nails of the ambulopus have fused into a single "hoof" that extends part of the way into the foot of the styloctopus. This intrusion connects with the cartilage skeleton of the leg to form a sort of pseudo-knee. Protrusions on the stylets have developed to better transfer weight onto the leg skeletons. The limbs no longer sprawl to the side but are carried directly beneath the animal.

The front pair of arms remain largely the same, long hooked appendages used for grasping food. The second pair of arms have shortened and become stubs used for holding food against the beak. The denticles of the second pair are used for chewing to a certain extent.

The siphon now acts to actively pump air across the gills, giving the mantle cavity the function of a circulatory lung like seen in birds. A swelling of the oviduct now retains offspring until hatching. The styloctopus gives live birth but does not possess a placenta and so is considered ovoviviparous.

The pupils of styloctopus are fully round. The behaviour of the styloctopus clade is wide and varied. The reproductive system of the styloctopus will likely continue to develop to include amniotic eggs, placental nourishment or other means. The primitive skeleton of the styloctopus will also continue to develop to suit new dangers and habitats. Continued specialisation of its limbs open new possibilities for styloctopus evolution.

If you've made it this far, thank you for reading.

I hope you enjoyed coming along for this journey as much as I did creating it. Speculative evolution is a fascinating field full of awe and wonder. I hope I managed to capture some of that with my take on the land cephalopod.