Hagfish

Hagfish, of the class Myxini (also known as Hyperotreti), are eel-shaped, slime-producing marine fish (occasionally called slime eels). They are the only known living animals that have a skull but no vertebral column, although hagfish do have rudimentary vertebrae.[3] Along with lampreys, hagfish are jawless; they are the sister group to jawed vertebrates, and living hagfish remain similar to hagfish from around 300 million years ago.[4]

Hagfish
Pacific hagfish resting on the ocean bottom, at 280 m depth off the Oregon coast
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Subphylum: Vertebrata
Superclass: Cyclostomata
Class: Myxini
Order: Myxiniformes
Family: Myxinidae
Rafinesque, 1815
Genera[1]
  • Rubicundinae Fernholm et al., 2013
    • Rubicundus Fernholm et al., 2013
  • Eptatretinae Bonaparte, 1850
    • Eptatretus Cloquet, 1819
  • Myxininae Nelson, 1976
    • Myxine Linnaeus, 1758
    • Nemamyxine Richardson, 1958
    • Neomyxine Richardson, 1953
    • Notomyxine Nani & Gneri, 1951
Synonyms
  • Bdellostomatidae Gill, 1872
  • Homeidae Garman, 1899
  • Paramyxinidae Berg, 1940
  • Diporobranchia Latreille, 1825[2]

The classification of hagfish had been controversial. The issue was whether the hagfish was a degenerate type of vertebrate-fish that through evolution had lost its vertebrae (the original scheme) and was most closely related to lampreys, or whether hagfish represent a stage that precedes the evolution of the vertebral column (the alternative scheme) as is the case with lancelets. Recent DNA evidence has supported the original scheme.[5]

The original scheme groups hagfish and lampreys together as cyclostomes (or historically, Agnatha), as the oldest surviving class of vertebrates alongside gnathostomes (the now-ubiquitous jawed vertebrates). The alternative scheme proposed that jawed vertebrates are more closely related to lampreys than to hagfish (i.e., that vertebrates include lampreys but exclude hagfish), and introduces the category craniata to group vertebrates near hagfish.

Physical characteristics
Two views of the hagfish (Myxini glutinosa) with analytical overlays and dissection, published 1905

Body features

Hagfish are typically about 0.5 m (19.7 in) in length. The largest known species is Eptatretus goliath, with a specimen recorded at 127 cm (4 ft 2 in), while Myxine kuoi and Myxine pequenoi seem to reach no more than 18 cm (7.1 in). Some have been seen as small as 4 cm (1.6 in).

Hagfish have elongated, eel-like bodies, and paddle-like tails. The skin is naked and covers the body like a loosely fitting sock. They have cartilaginous skulls (although the part surrounding the brain is composed primarily of a fibrous sheath) and tooth-like structures composed of keratin. Colors depend on the species, ranging from pink to blue-grey, and black or white spots may be present. Eyes are simple eyespots, not lensed eyes that can resolve images. Hagfish have no true fins and have six or eight barbels around the mouth and a single nostril. Instead of vertically articulating jaws like Gnathostomata (vertebrates with jaws), they have a pair of horizontally moving structures with tooth-like projections for pulling off food. The mouth of the hagfish has two pairs of horny, comb-shaped teeth on a cartilaginous plate that protracts and retracts. These teeth are used to grasp food and draw it toward the pharynx.[6]

Pacific hagfish at 150 m depth, California, Cordell Bank National Marine Sanctuary

Its skin is only attached to the body along the center ridge of the back and at the slime glands, and is filled with close to a third of the body's blood volume, giving the impression of a blood-filled sack. It is assumed this is an adaptation to survive predator attacks.[7] The Atlantic hagfish, representative of the subfamily Myxininae, and the Pacific hagfish, representative of the subfamily Eptatretinae, differ in that the latter has muscle fibers embedded in the skin. The resting position of the Pacific hagfish also tends to be coiled, while that of the Atlantic hagfish is stretched.[8][9]

Slime
Pacific hagfish trying to hide under a rock

Hagfish are long and vermiform, and can exude copious quantities of a milky and fibrous slime or mucus from some 100 glands or invaginations running along their flanks.[10] The species Myxine glutinosa was named for this slime. When captured and held, e.g., by the tail, they secrete the microfibrous mucus, which expands into up to 20 litres (5¼ US gallons) of sticky, gelatinous material when combined with water;[11] one litre of slime has about 40 milligrams of mucus and proteins.[12] If they remain captured, they can tie themselves in an overhand knot, which works its way from the head to the tail of the animal, scraping off the slime as it goes and freeing them from their captor. This singular behavior may assist them in extricating themselves from the jaws of predatory fish or from the interior of their own prey, and the sliming might act as a distraction to predators.[12]

Recently, the slime was reported to entrain water in its keratin-like intermediate filaments, creating a slow-to-dissipate, viscoelastic substance, rather than a simple gel. It has been proven to impair the function of a predator fish's gills. In this case, the hagfish's mucus would clog the predator's gills, disabling their ability to respire. The predator would release the hagfish to avoid suffocation. Because of the mucus, few marine predators target the hagfish. Other predators of hagfish are varieties of birds or mammals.[13]

Free-swimming hagfish also slime when agitated, and later clear the mucus using the same travelling-knot behavior.[14][15] The reported gill-clogging effect suggests that the travelling-knot behavior is useful or even necessary to restore the hagfish's own gill function after sliming.

Hagfish thread keratin (EsTKα and EsTKγ; Q90501 and Q90502), the protein that make up its slime filaments, is under investigation as an alternative to spider silk for use in applications such as body armor.[16] These alpha-keratin proteins in hagfish slime transform from an α-helical structure to a stiffer β sheet structure when stretched.[17] With combined draw-processing (stretching) and chemical crosslinking, recombinant slime keratin turns into a very strong fiber with stiffness reaching 20 GPa.[18]

Respiration

A hagfish generally respires by taking in water through its pharynx, past the velar chamber, and bringing the water through the internal gill pouches, which can vary in number from five to 16 pairs, depending on species.[19] The gill pouches open individually, but in Myxine, the openings have coalesced, with canals running backwards from each opening under the skin, uniting to form a common aperture on the ventral side known as the branchial opening. The esophagus is also connected to the left branchial opening, which is therefore larger than the right one, through a pharyngocutaneous duct (esophageocutaneous duct), which has no respiratory tissue. This pharyngocutaneous duct is used to clear large particles from the pharynx, a function also partly taking place through the nasopharyngeal canal. In other species, the coalescence of the gill openings is less complete, and in Bdellostoma, each pouch opens separately to the outside like in lampreys.[20][21] The unidirectional water flow passing the gills is produced by rolling and unrolling velar folds located inside a chamber developed from the nasohypophyseal tract, and is operated by a complex set of muscles inserting into cartilages of the neurocranium, assisted by peristaltic contractions of the gill pouches and their ducts.[22] Hagfish also have a well-developed dermal capillary network that supplies the skin with oxygen when the animal is buried in anoxic mud, as well as a high tolerance for both hypoxia and anoxia, with a well developed anaerobic metabolism.[23] The skin has also been suggested to be capable of cutaneous respiration.[24]

Nervous system
Dorsal / left lateral views of dissected hagfish brain, scale bar added for size

The origins of the vertebrate nervous system is of considerable interest to evolutionary biologists, and cyclostomes (hagfish and lampreys) are an important group for answering this question. The complexity of the hagfish brain has been an issue of debate since the late 19th century, with some morphologists believing that they do not possess a cerebellum, while others believe that it is continuous with the midbrain.[25] It is now believed that the hagfish neuroanatomy is similar to that of lampreys.[26] A common feature of both cyclostomes is the absence of myelin in neurons.[27]

Eye

The hagfish's eye, which lacks a lens, extraocular muscles, and the three motor cranial nerves (III, IV, and VI), is significant to the evolution of more complex eyes. A parietal eye and the parapineal organ are also absent in extant hagfish.[28][29] Hagfish eyespots, when present, can detect light, but as far as it is known, none can resolve detailed images. In Myxine and Neomyxine, the eyes are partly covered by the trunk musculature.[6] Paleontological evidence suggests, however, that the hagfish eye is not pleisiomorphic but rather degenerative, as fossils from the Carboniferous have revealed hagfish-like vertebrates with complex eyes. This would suggest that ancestrally Myxini possessed complex eyes.[30][31]

Cardiac function, circulation, and fluid balance

Hagfish are known to have one of the lowest blood pressures among the vertebrates.[32] One of the most primitive types of fluid balance found is among these creatures, whenever a rise in extracellular fluid occurs, the blood pressure rises and this, in turn, is sensed by the kidney, which excretes excess fluid.[23] They also have the highest blood volume to body mass of any chordate, with 17 ml of blood per 100 g of mass. [33]

The hagfish circulatory system has been of considerable interests to evolutionary biologists, who first believed that the hagfish heart was not innervated like that in jawed vertebrates.[34] Further investigation revealed that the hagfish did have a true innervated heart. The hagfish circulatory system also consists of multiple accessory pumps throughout the body, which are considered auxiliary “hearts”.[32]

Hagfish are the only known vertebrates with osmoregulation isosmotic to their external environment. Hypothetically, they excrete ions in bile salts.[35]

Musculoskeletal system

Hagfish musculature differs from jawed vertebrates in that they do not have a horizontal septum nor vertical septum, junctions of connective tissue that separate the hypaxial musculature and epaxial musculature. They do, however, have true myomeres and myosepta like all vertebrates. The mechanics of their craniofacial muscles in feeding have been investigated, revealing advantages and disadvantages of the dental plate. In particular, hagfish muscles have increased force and gape size compared to similar-sized jawed vertebrates, but lack the speed amplification, suggesting that jaws are faster acting.[36]

Horizontal section of hagfish midline trunk: The notochord is the only skeletal element and the musculature lacks a horizontal and vertical septum.

The hagfish skeleton comprises the skull, the notochord, and the caudal fin rays. The first diagram of the hagfish endoskeleton was made by Frederick Cole in 1905.[37] In Cole's monograph, he described sections of the skeleton that he termed "pseudo-cartilage", referring to its distinct properties compared to jawed chordates. The lingual apparatus of hagfish is composed of a cartilage base bearing two teeth-covered plates (dental plate) articulated with a series of large cartilage shafts. The nasal capsule is considerably expanded in hagfish, comprising a fibrous sheath lined with cartilage rings. In contrast to lampreys, the braincase is noncartilaginous. The role of the branchial arches is highly speculative, as hagfish embryos undergo a caudal shift of the posterior pharyngeal pouches; thus, the branchial arches do not support gills.[38] While parts of the hagfish skull are thought to be homologous with lampreys, they are thought to have very few homologous elements with jawed vertebrates.[39]

Reproduction
Drawing of Eptatretus polytrema
Drawing of a New Zealand hagfish

Very little is known about hagfish reproduction. Embryos are difficult to obtain for study, although laboratory breeding of the Far Eastern inshore hagfish, Eptatretus burgeri, has succeeded.[40] In some species, sex ratio has been reported to be as high as 100:1 in favor of females. Some hagfish species are thought to be hermaphroditic, having both an ovary and a testicle (only one gamete production organ is in both females and males). In some cases, the ovary is thought to remain nonfunctional until the individual has reached a particular age or encounters a particular environmental stress. These two factors in combination suggest the survival rate of hagfish is quite high.

Depending on species, females lay from one to 30 tough, yolky eggs. These tend to aggregate due to having Velcro-like tufts at either end. Hagfish are sometimes seen curled around small clutches of eggs. If this constitutes actual breeding behavior is uncertain.

Hagfish do not have a larval stage, in contrast to lampreys, which have a long one.

Hagfish have a mesonephric kidney and are often neotenic of their pronephric kidney. The kidney(s) are drained via mesonephric/archinephric duct. Unlike many other vertebrates, this duct is separate from the reproductive tract. Unlike all other vertebrates, the proximal tubule of the nephron is also connected with the coelom, provided lubrication.

The single testicle or ovary has no transportation duct. Instead, the gametes are released into the coelom until they find their way to the posterior end of the caudal region, whereby they find an opening in the digestive system.

Development of the hagfish embryo is retarded in comparison to other jawless vertebrates, taking as long as 11 months before hatching.[41] Thus, information on their embryology has been obscured until recently, when husbandry advances have enabled considerable advances to the understanding of the group's evolutionary development. Their development has provided new insights into the evolution of neural crest cells, solidifying the consensus that these cells are a shared trait by all vertebrates and that are regulated by a common subset of genes.[42]

The inshore hagfish is the only member of the hagfish family with a seasonal reproductive cycle.[43]

Feeding
Two Pacific hagfish feeding on a dead sharpchin rockfish, Sebastes zacentrus, while one remains in a curled position at the left of the photo

While polychaete marine worms on or near the sea floor are a major food source, hagfish can feed upon and often even enter and eviscerate the bodies of dead and dying/injured sea creatures much larger than themselves. They are known to devour their prey from the inside.[44] Hagfish have the ability to absorb dissolved organic matter across the skin and gill, which may be an adaptation to a scavenging lifestyle, allowing them to maximize sporadic opportunities for feeding. From an evolutionary perspective, hagfish represent a transitory state between the generalized nutrient absorption pathways of aquatic invertebrates and the more specialized digestive systems of aquatic vertebrates.[45]

Like leeches, they have a sluggish metabolism and can survive months between feedings;[46][47] their feeding behavior, however, appears quite vigorous. Analysis of the stomach content of several species has revealed a large variety of prey, including polychaetes, shrimp, hermit crabs, cephalopods, brittlestars, bony fishes, sharks, birds, and whale flesh.[48]

In captivity, hagfish are observed to use the overhand-knot behavior in reverse (tail-to-head) to assist them in gaining mechanical advantage to pull out chunks of flesh from carrion fish or cetaceans, eventually making an opening to permit entry to the interior of the body cavity of larger carcasses. A healthy larger sea creature likely would be able to outfight or outswim this sort of assault.

This energetic opportunism on the part of the hagfish can be a great nuisance to fishermen, as they can devour or spoil entire deep drag-netted catches before they can be pulled to the surface. Since hagfish are typically found in large clusters on and near the bottom, a single trawler's catch could contain several dozen or even hundreds of hagfish as bycatch, and all the other struggling, captive sea life make easy prey for them.

The digestive tract of the hagfish is unique among the chordates because the food in the gut is enclosed in a permeable membrane, analogous to the peritrophic matrix of insects.[49]

Hagfish have also been observed actively hunting the red bandfish, Cepola haastii, in its burrow, possibly using their slime to suffocate the fish before grasping it with their dental plates and dragging it from the burrow.[50]

Classification

Originally, Myxine was included by Linnaeus (1758) in Vermes. A single fossil of hagfish shows little evolutionary change has occurred in the last 300 million years.[51] In recent years, hagfish have become of special interest for genetic analysis investigating the relationships among chordates. Their classification as agnathans places hagfish as elementary vertebrates in between invertebrates and gnathostomes. However, discussion has long occurred in scientific literature about whether the hagfish were even invertebrate. Using fossil data, paleontologists posited that lampreys are more closely related to gnathostomes than hagfish. The term “Craniata” was used to refer to animals that had a developed skull, but were not considered true vertebrates.[52] Molecular evidence in the early 1990s first began suggesting that lampreys and hagfish were more closely related to each other than to gnathostomes.[53] The validity of the taxon "Craniata" was further examined by Delarbre et al. (2002) using mtDNA sequence data, concluding the Myxini are more closely related to the Hyperoartia than to the Gnathostomata – i.e., that modern jawless fishes form a clade called the Cyclostomata. The argument is that if the Cyclostomata are indeed monophyletic, Vertebrata would return to its old content (Gnathostomata + Cyclostomata) and the name Craniata, being superfluous, would become a junior synonym.[5] Nowadays, molecular data are almost unanimously in consensus of cyclostome monophyly, with more recent work being directed at shared microRNAs between cyclostomes and gnathostomes.[54] The current classification supported by molecular analyses (which show that lampreys and hagfishes are sister taxa), as well as the fact that hagfishes do, in fact, have rudimentary vertebrae, which places hagfishes in Cyclostomata.[3]

Phylogeny

The following hagfish and lamprey phylogeny is an adaptation based on the 2006 work by Shigeru Kuratani and Shigehiro Kuraku:[55]

Simplified cyclostome phylogeny based on the work of Shigeru Kuratani and Shigehiro Kuraku:[55]

Commercial use
Kkomjangeo bokkeum (꼼장어 볶음), Korean stir-fried fish dish made with the hagfish Eptatretus burgeri

As food

In most of the world, Hagfish are not often eaten. In Korea, the hagfish is a valued food, where it is generally skinned, coated in spicy sauce, and grilled over charcoal or stir-fried. It is especially popular in the southern port cities of the peninsula, such as Busan. The inshore hagfish, found in the Northwest Pacific, is eaten in Japan.[43] As hagfish slime binds vast amounts of liquid even at low temperatures, it was proposed as an energy-saving alternative for the production of tofu that does not require heating.[56]

Skins

Hagfish skin, used in a variety of clothing accessories, is usually referred to as "eel skin". It produces a particularly durable leather, especially suitable for wallets and belts.[57]

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