Lamprey

Adults superficially resemble eels in that they have scaleless, elongated bodies, and can range from 13 to 100 cm (5 to 39.5 in) in length. Lacking paired fins, adult lampreys have large eyes, one nostril atop the head, and seven gill pores on each side of the head.

The brain of the lamprey is divided into the telencephalon, diencephalon, midbrain, cerebellum, and medulla.[14]

The heart of the lamprey is anterior to the intestines. It contains the sinus, one atrium, and one ventricle protected by the pericardial cartilages.[14]

The pineal gland, a photosensitive organ regulating melatonin production by capturing light signals through the photoreceptor cell converting them into intercellular signals of the lamprey is located in the midline of its body, for lamprey, the pineal eye is accompanied by the parapineal organ.[15]

The buccal cavity, anterior to the gonads, is responsible for attaching the animal, through suction, to either a stone or its prey. This then allows the tongue to make contact with the stone to rasp algae, or tear at the flesh of their prey to yield blood.[16]

The pharynx is subdivided; the ventral part forming a respiratory tube that is isolated from the mouth by a valve called the velum. This is an adaptation to how the adults feed, by preventing the prey's body fluids from escaping through the gills or interfering with gas exchange, which takes place by pumping water in and out of the gill pouches instead of taking it in through the mouth.

One of the key physical components to the lamprey are the intestines, which are located ventral to the notochord. Intestines aid in osmoregulation by intaking water from its environment and desalinating the water they intake to an iso-osmotic state with respect to blood, and are also responsible for digestion.[17]

Near the gills are the eyes, which are poorly developed and buried under skin in the larvae. The eyes consummate their development during metamorphosis, and are covered by a thin and transparent layer of skin that becomes opaque in preservatives.[18]

The cartilaginous skeleton of a lamprey washed up on a beach in North Carolina.

The unique morphological characteristics of lampreys, such as their cartilaginous skeleton, suggest they are the sister taxon (see cladistics) of all living jawed vertebrates (gnathostomes). They are usually considered the most basal group of the Vertebrata. Instead of true vertebrae, they have a series of cartilaginous structures called arcualia arranged above the notochord. Hagfish, which resemble lampreys, have traditionally been considered the sister taxon of the true vertebrates (lampreys and gnathostomes)[19] but DNA evidence suggests that they are in fact the sister taxon of lampreys.[20]

Studies have shown that lampreys are among the most energy-efficient swimmers. Their swimming movements generate low-pressure zones around the body, which pull rather than push their bodies through the water.[21]

Research on sea lampreys has revealed that sexually mature males use a specialized heat-producing tissue in the form of a ridge of fat cells near the anterior dorsal fin to stimulate females. After having attracted a female with pheromones, the heat detected by the female through body contact will encourage spawning.[22]

Due to certain peculiarities in their adaptive immune system, the study of lampreys provides valuable insight into the evolution of vertebrate adaptive immunity. Generated from a somatic recombination of leucine-rich repeat gene segments, lamprey leukocytes express surface variable lymphocyte receptors (VLRs).[23] This convergently evolved characteristic allows them to have lymphocytes that work as the T cells and B cells present in higher vertebrates immune system.[24]

Northern lampreys (Petromyzontidae) have the highest number of chromosomes (164–174) among vertebrates.[25]

Pouched lamprey (Geotria australis) larvae also have a very high tolerance for free iron in their bodies, and have well-developed biochemical systems for detoxification of the large quantities of these metal ions.[26]

Lampreys are the only extant vertebrate to have four eyes.[27] Most lampreys have two additional parietal eyes: a pineal and parapineal one (the exception is members of Mordacia).[28]

Different species of lamprey have many shared physical characteristics. The same anatomical structure can serve different functions in the lamprey depending on whether or not it is carnivorous. For example, non-carnivorous species use their teeth to scrape algae from rocks for food,[29] rather than drilling into the flesh of hosts. The mouth and suction capabilities of the lamprey not only allow it to cling to a fish as a parasite,[30] but provide it with limited climbing ability so that it can travel upstream and up ramps or rocks to breed.[31][30] This ability has been studied in an attempt to better understand how lampreys battle the current and move forward despite only being able to hold onto the rock at a single point.[31] Some scientists are also hoping to design ramps[31] that will optimize the lamprey's climbing ability, as lampreys are valued as food in the Northwest United States and need to travel upstream to reproduce.[30]

The last common ancestor of lampreys appears to have been specialized to feed on the blood and body fluids of other fish after metamorphosis.[32] They attach their mouthparts to the target animal's body, then use three horny plates (laminae) on the tip of their piston-like tongue, one transversely and two longitudinally placed, to scrape through surface tissues until they reach body fluids.[33] The teeth on their oral disc are primarily used to help the animal attach itself to its prey.[34] Made of keratin and other proteins, lamprey teeth have a hollow core to give room for replacement teeth growing under the old ones.[35] Some of the original blood-feeding forms have evolved into species that feed on both blood and flesh, and some who have become specialized to eat flesh and may even invade the internal organs of the host. Tissue feeders can also involve the teeth on the oral disc in the excision of tissue.[36] As a result, the flesh-feeders have smaller buccal glands as they do not require the production of anticoagulant continuously and mechanisms for preventing solid material entering the branchial pouches, which could otherwise potentially clog the gills.[37] A study of the stomach content of some lampreys has shown the remains of intestines, fins and vertebrae from their prey.[38] Although attacks on humans do occur,[39] they will generally not attack humans unless starved.[40][19]

Carnivorous forms have given rise to the non-carnivorous species that feed on algae,[41] and "giant" individuals amongst the otherwise small American brook lamprey have occasionally been observed, leading to the hypothesis that sometimes individual members of non-carnivorous forms return to the carnivorous lifestyle of their ancestors.[42]

The lamprey's light-colored underside and darker back allow it to blend in when viewed from above or below, an example of countershading

Another important lamprey adaptation is its countershading, a form of camouflage. Similarly to many other aquatic species, most lampreys have a dark-colored back, which enables them to blend in with the ground below when seen from above by a predator. Their light-colored undersides allow them to blend in with the bright air and water above them if a predator sees them from below.

Lamprey coloration can also vary according to the region and specific environment in which the species is found. Some species can be distinguished by their unique markings – for example, Geotria australis individuals display two bluish stripes running the length of its body as an adult.[43] These markings can also sometimes be used to determine what stage of the life cycle the lamprey is in; G. australis individuals lose these stripes when they approach the reproductive phase and begin to travel upstream.[43] Another example is Petromyzon marinus, which shifts to more of an orange color as it reaches the reproductive stage in its life cycle.

Larva of an unknown lamprey species

The adults spawn in nests of sand, gravel and pebbles in clear streams. After hatching from the eggs, young larvae—called ammocoetes[44][45]—will drift downstream with the current till they reach soft and fine sediment in silt beds, where they will burrow in silt, mud and detritus, taking up an existence as filter feeders, collecting detritus, algae, and microorganisms.[46] The eyes of the larvae are underdeveloped, but are capable of discriminating changes in illuminance.[47] Ammocoetes can grow from 3–4 inches (8–10 centimetres) to about 8 inches (20 cm).[48][49] Many species change color during a diurnal cycle, becoming dark at day and pale at night.[50] The skin also has photoreceptors, light sensitive cells, most of them concentrated in the tail, which helps them to stay buried.[51] Lampreys may spend up to eight years as ammocoetes,[52] while species such as the Arctic lamprey may only spend one to two years as larvae,[53] prior to undergoing a metamorphosis which generally lasts 3–4 months, but can vary between species.[54] While metamorphosing, they do not eat.[55]

The rate of water moving across the ammocoetes' feeding apparatus is the lowest recorded in any suspension feeding animal, and they therefore require water rich in nutrients to fulfill their nutritional needs. While the majority of (invertebrate) suspension feeders thrive in waters containing under 1 mg suspended organic solids per litre (<1 mg/L), ammocoetes demand minimum 4 mg/L, with concentrations in their habitats having been measured up to 40 mg/L.[56]

During metamorphosis the lamprey loses both the gallbladder and the biliary tract,[57] and the endostyle turns into a thyroid gland.[58]

Some species, including those that are not carnivorous and do not feed even following metamorphosis,[55] live in freshwater for their entire lifecycle, spawning and dying shortly after metamorphosing.[59] In contrast, many species are anadromous and migrate to the sea,[55] beginning to prey on other animals while still swimming downstream after their metamorphosis provides them with eyes, teeth, and a sucking mouth.[60][59] Those that are anadromous are carnivorous, feeding on fishes or marine mammals.[10][61][62]

Anadromous lampreys spend up to four years in the sea before migrating back to freshwater, where they spawn. Adults create nests (called redds) by moving rocks, and females release thousands of eggs, sometimes up to 100,000.[59] The male, intertwined with the female, fertilizes the eggs simultaneously. Being semelparous, both adults die after the eggs are fertilized.[63]

Jamoytius kerwoodi, a putative lamprey relative from the Silurian

Mayomyzon, one of the oldest known lampreys

Lamprey fossils are rare because cartilage fossilizes less readily than bone. The first fossil lampreys were originally found in Early Carboniferous limestones, marine sediments in North America: Mayomyzon pieckoensis and Hardistiella montanensis, from the Mississippian Mazon Creek lagerstätte and the Bear Gulch Limestone sequence. None of the fossil lampreys found to date have been longer than 10 cm (4 in),[75] and all the Paleozoic forms have been found in marine deposits.[76]

In the 22 June 2006 issue of Nature, Mee-mann Chang and colleagues reported on a fossil lamprey from the Yixian Formation of Inner Mongolia. The new species, morphologically similar to Carboniferous and other forms, was given the name Mesomyzon mengae ("Meng Qingwen's Mesozoic lamprey").

The exceedingly well-preserved fossil showed a well-developed sucking oral disk, a relatively long branchial apparatus showing a branchial basket, seven gill pouches, gill arches, and even the impressions of gill filaments, and about 80 myomeres of its musculature. Unlike the North American fossils, its habitat was almost certainly fresh water.[77]

Months later, a fossil lamprey even older than the Mazon Creek genera was reported from Witteberg Group rocks near Grahamstown, in the Eastern Cape of South Africa. Dating back 360 Million years, this species, Priscomyzon riniensis, is very similar to lampreys found today.[78][79][80] 310 to 360 million years old fossils of P. riniensis hatchlings indicate that the ammocoete larva is a more recent evolutionary trait among the lampreys. The hatchlings, measuring 15mm in length, still had their yolk sac, but were found in marine sediments and already had large eyes and a toothed suction disk.[81]

Portuguese lamprey rice

Yatsume kabayaki in Japan

Lampreys have long been used as food for humans.[90] They were highly appreciated by the ancient Romans. During the Middle Ages they were widely eaten by the upper classes throughout Europe, especially during Lent, when eating meat was prohibited, due to their meaty taste and texture. King Henry I of England is claimed to have been so fond of lampreys that he often ate them late into life and poor health against the advice of his physician concerning their richness, and is said to have died from eating "a surfeit of lampreys". Whether or not his lamprey indulgence actually caused his death is unclear.[91]

The pie made for the coronation of Elizabeth II of the United Kingdom on 4 March 1953 was a lamprey pie. However, after many decades, the city of Gloucester had to use Great Lakes lampreys for her Diamond Jubilee in 2012 because few lampreys could be found in the River Severn.[92][93]

In southwestern Europe (Portugal, Spain, and France), Finland and in Latvia (where lamprey is routinely sold in supermarkets), lampreys are a highly prized delicacy. In Finland (county of Nakkila),[94] and Latvia (Carnikava Municipality), the river lamprey is the local symbol, found on their coats of arms. In 2015 the lamprey from Carnikava was included in the Protected designation of origin list by the European Commission.[95]

Sea lamprey is the most sought-after species in Portugal and one of only two that can legally bear the commercial name "lamprey" (lampreia): the other one being Lampetra fluviatilis, the European river lamprey, both according to Portaria (Government regulation no. 587/2006, from 22 June). "Arroz de lampreia" or lamprey rice is one of the most important dishes in Portuguese cuisine.

The European river lamprey in the coat of arms of Nakkila, Finland. Lampreys are a traditional delicacy in locality.[96]

Lampreys are also consumed in Sweden, Russia, Lithuania, Estonia, Japan, and South Korea. In Finland, they are commonly eaten grilled or smoked, but also pickled, or in vinegar.[97]

The mucus and serum of several lamprey species, including the Caspian lamprey (Caspiomyzon wagneri), river lampreys (Lampetra fluviatilis and L. planeri), and sea lamprey (Petromyzon marinus), are known to be toxic, and require thorough cleaning before cooking and consumption.[98][99]

In Britain, lampreys are commonly used as bait, normally as dead bait. Northern pike, perch, and chub all can be caught on lampreys. Frozen lampreys can be bought from most bait and tackle shops.

Lampreys attached to a lake trout.

Sea lampreys have become a major pest in the North American Great Lakes. It is generally believed that they gained access to the lakes via canals during the early 20th century,[100][101] but this theory is controversial.[102] They are considered an invasive species, have no natural enemies in the lakes, and prey on many species of commercial value, such as lake trout.[100]

Lampreys are now found mostly in the streams that feed the lakes, and controlled with special barriers to prevent the upstream movement of adults, or by the application of toxicants called lampricides, which are harmless to most other aquatic species; however, these programs are complicated and expensive, and do not eradicate the lampreys from the lakes, but merely keep them in check.[103]

New programs are being developed, including the use of chemically sterilized male lampreys in a method akin to the sterile insect technique.[104] Finally, pheromones critical to lamprey migratory behaviour have been isolated, their chemical structures determined, and their impact on lamprey behaviour studied, in the laboratory and in the wild, and active efforts are underway to chemically source and to address regulatory considerations that might allow this strategy to proceed.[105][106][107]

Control of sea lampreys in the Great Lakes is conducted by the U.S. Fish and Wildlife Service and the Canadian Department of Fisheries and Oceans, and is coordinated by the Great Lakes Fishery Commission.[108] Lake Champlain, bordered by New York, Vermont, and Quebec, and New York's Finger Lakes are also home to high populations of sea lampreys that warrant control.[109] Lake Champlain's lamprey control program is managed by the New York State Department of Environmental Conservation, the Vermont Department of Fish and Wildlife, and the U.S. Fish and Wildlife Service.[109] New York's Finger Lakes sea lamprey control program is managed solely by the New York State Department of Environmental Conservation.[109]

In folklore, lampreys are called "nine-eyed eels". The name is derived from the seven external gill slits that, along with one nostril and one eye, line each side of a lamprey's head section. Likewise, the German word for lamprey is Neunauge, which means "nine-eye",[110] and in Japanese they are called yatsume-unagi (八つ目鰻, "eight-eyed eels"), which excludes the nostril from the count. In British folklore, the monster known as the Lambton Worm may have been based on a lamprey, since it is described as an eel-like creature with nine eyes.

Illustration from an edition of Tacuinum Sanitatis, 15th century

Vedius Pollio kept a pool of lampreys into which slaves who incurred his displeasure would be thrown as food.[111] On one occasion, Vedius was punished by Augustus for attempting to do so in his presence:

... one of his slaves had broken a crystal cup. Vedius ordered him to be seized and then put to death, but in an unusual way. He ordered him to be thrown to the huge lampreys which he had in his fish pond. Who would not think he did this for display? Yet it was out of cruelty. The boy slipped from the captor's hands and fled to Augustus's feet asking nothing else other than a different way to die – he did not want to be eaten. Augustus was moved by the novelty of the cruelty and ordered him to be released, all the crystal cups to be broken before his eyes, and the fish pond to be filled in ...

— Seneca, On Anger, III, 40[112]

This incident was incorporated into the plot of the 2003 novel Pompeii by Robert Harris in the incident of Ampliatus feeding a slave to his lampreys.

Lucius Licinius Crassus was mocked by Gnaeus Domitius Ahenobarbus (cos. 54 BC) for weeping over the death of his pet lamprey:

So, when Domitius said to Crassus the orator, Did not you weep for the death of the lamprey you kept in your fish pond? – Did not you, said Crassus to him again, bury three wives without ever shedding a tear? – Plutarch, On the Intelligence of Animals, 976a[113]

This story is also found in Aelian (Various Histories VII, 4) and Macrobius (Saturnalia III.15.3). It is included by Hugo von Hofmannsthal in the Chandos Letter:

And in my mind I compare myself from time to time with the orator Crassus, of whom it is reported that he grew so excessively enamoured of a tame lamprey – a dumb, apathetic, red-eyed fish in his ornamental pond – that it became the talk of the town; and when one day in the Senate Domitius reproached him for having shed tears over the death of this fish, attempting thereby to make him appear a fool, Crassus answered, "Thus have I done over the death of my fish as you have over the death of neither your first nor your second wife." I know not how oft this Crassus with his lamprey enters my mind as a mirrored image of my Self, reflected across the abyss of centuries.

— Philip, Lord Chandos, (fictional) younger son of the Earl of Bath, in a letter to Francis Bacon[114]

In George R. R. Martin's novel series, A Song of Ice and Fire, Lord Wyman Manderly is mockingly called "Lord Lamprey" by his enemies in reference to his rumored affinity to lamprey pie and his striking obesity.[115]

Kurt Vonnegut, in his late short story "The Big Space Fuck", posits a future America so heavily polluted – "Everything had turned to shit and beer cans", in his words – that the Great Lakes have been infested with a species of massive, man-eating ambulatory lampreys.[116]

In season 3, episode 5 of “The Borgias”, whilst out on a hunting trip, Cesare Borgia’s mercenary, Micheletto, kills the King of Naples by pushing him into a pool filled with lampreys that King Firante had built during his reign of Naples.[117]

• Renaud, C.B. (2011) Lampreys of the world. An annotated and illustrated catalogue of lamprey species known to date FAO Species Catalogue for Fishery Purposes. No. 5. Rome. ISBN 978-92-5-106928-8.

• Sorensen, Peter W.; Fine, Jared M.; Dvornikovs, Vadims; Jeffrey, Christopher S.; Shao, Feng; Wang, Jizhou; Vrieze, Lance A.; Anderson, Kari R.; Hoye, Thomas R. (2005). "Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey". Nature Chemical Biology. 1 (6): 324–328. doi:10.1038/nchembio739. PMID 16408070. S2CID 43298112., see Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey, accessed 1 July 2015. [Primary source example.]
• Dittman, Andrew (2005). "News and Views: Chemical cues for sea lamprey migration". Nature Chemical Biology (Submitted manuscript). 1 (6): 316–317. doi:10.1038/nchembio1105-316. PMID 16408065. S2CID 42664483., see Chemical cues for sea lamprey migration, accessed 1 July 2015. [Lay summary of Sorensen, et al. (2005)]
• Johnson, Nicholas S.; Yun, Sang-Seon; Thompson, Henry T.; Brant, Cory O.; Li, Weiming (2009). "A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps". Proceedings of the National Academy of Sciences. 106 (4): 1021–1026. doi:10.1073/pnas.0808530106. PMC 2633527. PMID 19164592. [Primary source example.]
• Richard Black, 2009, "Sex smell lures 'vampire' to doom," BBC News (online), 20 January 2009, see Sex smell lures 'vampire' to doom, accessed 1 July 2015. [Lay summary of Johnson, et al. (2009); Subtitle: "A synthetic 'chemical sex smell' could help rid North America's Great Lakes of a devastating pest, scientists say."]