Lamprey

For other uses, see Lamprey (disambiguation).
Lamprey
Temporal range: Late Devonian–Holocene

[1]

A European river lamprey (Lampetra fluviatilis)
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Hyperoartia
Order: Petromyzontiformes
Berg, 1940[2]
Families

† = extinct

Mouth of a sea lamprey, Petromyzon marinus
Microscopic cross section through the pharynx of a larva from an unknown lamprey species

Lampreys (sometimes also called, inaccurately, lamprey eels) are any jawless fish of the order Petromyzontiformes, placed in the superclass Cyclostomata. The adult lamprey may be characterized by a toothed, funnel-like sucking mouth. The common name "lamprey" is probably derived from Latin lampetra, which may mean "stone licker" (lambere "to lick" + petra "stone"), though the etymology is uncertain.[3]

Currently there are about 38 known extant species of lampreys.[4] Although they are well known for boring into the flesh of other fish to suck their blood,[5] only 18 species of lampreys are actually parasitic.[6] The lampreys are a very ancient lineage of vertebrates, though their exact relationship to hagfishes and jawed vertebrates is still a matter of dispute.

Characteristics

Adults superficially resemble eels in that they have scaleless, elongated bodies, and can range from 13 to 100 cm (5 to 40 inches) in length. Lacking paired fins, adult lampreys have large eyes, one nostril on the top of the head, and seven gill pores on each side of the head. 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), and 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. Parasitic lampreys feed on prey as adults by attaching their mouthparts to the target animal's body, then using their teeth to cut through surface tissues until they reach blood and body fluid. Although attacks on humans do occur,[7] they will generally not attack humans unless starved.[8][9] Non-parasitic lampreys, which are usually freshwater species, do not feed as adults; they live off reserves acquired as ammocoetes (larvae), which they obtain through filter feeding.[10]

Hagfish, which resemble lampreys, have traditionally been considered the sister taxon of the true vertebrates (lampreys and gnathostomes)[9] but DNA evidence suggests that they are in fact the sister taxon of lampreys.

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. Near the gills are the eyes, which are poorly developed and buried under skin in the larvae. The eyes complete their development during metamorphosis, and in adults are covered by a thin and transparent layer of skin that becomes opaque in preservatives.[11]

Lampreys provide valuable insight into adaptive immune systems, as they possess a convergently evolved adaptive immunity with cells that function like the T cells and B cells seen in higher vertebrates. Lamprey leukocytes express surface variable lymphocyte receptors (VLRs) generated from somatic recombination of leucine-rich repeat gene segments in a recombination activating gene-independent manner.[12][13]

Northern lampreys (Petromyzontidae) have the highest number of chromosomes (164–174) among vertebrates.[14]

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.[15]

Research

Stimulation of the olfactory sensory neurons in the periphery activates neurons in the olfactory bulb of a sea lamprey[16]

The lamprey has been extensively studied because its relatively simple brain is thought in many respects to reflect the brain structure of early vertebrate ancestors. Beginning in the 1970s, Sten Grillner and his colleagues at the Karolinska Institute in Stockholm have used the lamprey as a model system to work out the fundamental principles of motor control in vertebrates, starting in the spinal cord and working toward the brain.[17] In a series of studies, they found neural circuits within the spinal cord are capable of generating the rhythmic motor patterns that underlie swimming; these circuits are controlled by specific locomotor areas in the brainstem and midbrain; and these areas, in turn, are controlled by higher brain structures, including the basal ganglia and tectum. In a study of the lamprey tectum published in 2007,[18] they found electrical stimulation could elicit eye movements, lateral bending movements, or swimming activity, and the type, amplitude, and direction of movement varied as a function of the location within the tectum that was stimulated. These findings were interpreted as consistent with the idea that the tectum generates goal-directed locomotion in the lamprey as it does in other species.

Lampreys are used as a model organism in biomedical research, where their large reticulospinal axons are used to investigate synaptic transmission.[19] The axons of lamprey are particularly large and allow for microinjection of substances for experimental manipulation.

Studies have shown that lampreys are amongst the most energy-efficient swimmers. Their swimming movements generate low-pressure zones around their body, which pull rather than push their bodies through the water.[20]

Distribution

Sea lamprey, Petromyzon marinus

Lampreys live mostly in coastal and fresh waters, although some species (e.g. Geotria australis, Petromyzon marinus, and Entosphenus tridentatus) travel significant distances in the open ocean,[21] as evidenced by their lack of reproductive isolation between populations. Some species are found in land-locked lakes. They are found in most temperate regions except those in Africa. Their larvae (ammocoetes) have a low tolerance for high water temperatures, which may explain why they are not distributed in the tropics.

Lamprey distribution may be adversely affected by overfishing and pollution. In Britain, at the time of the Conquest, lampreys were found as far upstream in the River Thames as Petersham . Reduction of pollution in the Thames and River Wear has led to recent sightings in London and Chester-le-Street.[22][23]

Distribution may also be adversely affected by dams and other construction projects disrupting migration routes, obstructing access to spawning grounds. Conversely, the construction of artificial channels has exposed new habitats for colonisation notably in North America where sea lampreys have become a significant introduced pest in the Great Lakes. Active control programs to control lampreys are undergoing modifications due to concerns of drinking water quality in some areas. [24]

Lifecycle

Larva of an unknown lamprey species

Adult lampreys spawn in rivers and then die. The young larvae, ammocoetes, spend several years in the rivers, where they live burrowed in fine sediment, filter feeding on detritus and microorganisms.[25] Then, ammocoetes undergo a metamorphosis lasting several months. Some species do not feed after metamorphosis, while others migrate to the sea or lakes,[26] where they feed on different species of fish and even on marine mammals.[21][27][28] Species whose adults migrate to the sea begin preying on other fish soon after metamorphosis, even as they begin swimming downstream.[29]

Taxonomy and systematics

Ammocoetes larva of Lethenteron reissneri
Several species of European lampreys
Pouched lamprey

Taxonomists place lampreys and hagfish in the subphylum Vertebrata of the phylum Chordata, which also includes the invertebrate subphyla Tunicata (sea-squirts) and the fish-like Cephalochordata (lancelets or Amphioxus). Recent molecular and morphological phylogenetic studies place lampreys and hagfish in the superclass Agnatha or Agnathostomata (both meaning without jaws). The other vertebrate superclass is Gnathostomata (jawed mouths) and includes the classes Chondrichthyes (sharks), Osteichthyes (bony fishes), Amphibia, Reptilia, Aves, and Mammalia.

Some researchers have classified lampreys as the sole surviving representatives of the Linnean class Cephalaspidomorphi.[30] Cephalaspidomorpha is sometimes given as a subclass of the Cephalaspidomorphi. Fossil evidence now suggests lampreys and cephalaspids acquired their shared characters by convergent evolution.[31][32] As such, many newer works, such as the fourth edition of Fishes of the World, classify lampreys in a separate group called Hyperoartia or Petromyzontida,[30] but whether this is actually a clade is disputed. Namely, it has been proposed that the non-lamprey "Hyperoartia" are in fact closer to the jawed vertebrates.

The debate about their systematics notwithstanding, lampreys constitute a single order Petromyzontiformes. Sometimes still seen is the alternative spelling "Petromyzoniformes", based on the argument that the type genus is Petromyzon and not "Petromyzonta" or similar. Throughout most of the 20th century, both names were used pretty much indiscriminately, even by the same author in subsequent publications. In the mid-1970s, the ICZN was called upon to fix one name or the other, and after much debate had to resolve the issue by voting. Thus, in 1980, the spelling with a "t" won out, and in 1981, it became official that all higher-level taxa based on Petromyzon have to start with "Petromyzont-".

The following taxonomy is based upon the treatment by FishBase as of April 2012 with phylogeny compiled by Mikko Haaramo.[33] Within the order are 10 living genera in three families. Two of the latter are monotypic at genus level today, and in one of them a single living species is recognized (though it may be a cryptic species complex):[34]
Hardistiellidae

?†Hardistiella montanensis Janvier & Lund 1983
Mayomyzonidae

†Mayomyzon pieckoensis Bardack & Zangerl 1962
Pipisciidae

?†Pipiscius zangerli Bardack & Richardson 1977

†Priscomyzon riniensis Gess, Coates & Rubidge 2006

†Mesomyzon mengae Chang, Zhang & Miao 2006


Petromyzontidae
Geotriinae

Geotria Gray 1851 (pouched lamprey)


Mordaciinae

Mordacia Gray 1853 (southern topeyed lampreys)


Petromyzontinae
Petromyzontini

Petromyzon Linnaeus 1758 (Sea lamprey)

Ichthyomyzon Girard 1858



Lampetrini

Caspiomyzon Berg 1906 (Caspian lamprey)

Tetrapleurodon Creaser & Hubbs 1922

Entosphenus Gill 1863

Lethenteron Creaser & Hubbs 1922

Eudontomyzon Regan 1911

Lampetra Bonnaterre 1788














Fossil record

Jamoytius kerwoodi, a putative lamprey relative from the Silurian
Mayomyzon, one of the oldest known lampreys

Lamprey fossils are rare because cartilage does not fossilize as readily as 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.

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.[35]

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. This species, Priscomyzon riniensis, is very similar to lampreys found today.[36][37][38]

As food

Portuguese lamprey rice

Lampreys have long been used as food for humans.[39] They were highly appreciated by ancient Romans. During the Middle Ages, they were widely eaten by the upper classes throughout Europe, especially during Lent when they were church-sanctioned food with a much meatier taste than that of most other fish. King Henry I of England is said to have died from eating "a surfeit of lampreys."[40]

On 4 March 1953, Queen Elizabeth II's coronation pie was made by the Royal Air Force using lampreys.[41]

In southwestern Europe (Portugal, Spain, and France) and in the northern half in Finland especially, larger lampreys are still a highly prized delicacy. 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). Overfishing has reduced their number in those parts. Lampreys are also consumed in Sweden, Finland, Russia, New Zealand, the Baltic countries, Japan, and South Korea.

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.[42][43]

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.

As pests

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,[44][45] but this theory is controversial.[46] 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.[44] 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, those programs are complicated and expensive, and do not eradicate the lampreys from the lakes, but merely keep them in check.[47] New programs are being developed, including the use of chemically sterilized male lampreys in a method akin to the sterile insect technique. 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.[48][49][50]

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. 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. 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. New York's Finger Lakes sea lamprey control program is managed solely by the New York State Department of Environmental Conservation.

Folklore

In folklore, lampreys are called "nine-eyed eels". The name is derived from the seven external gill slits which, 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".[51]

In literature

Illustration from an edition of Tacuinum Sanitatis, 15th century

Vedius Pollio was punished by Augustus for attempting to feed a clumsy slave to the lampreys in his fish pond. 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.

...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' 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[52]

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[53]

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, younger son of the Earl of Bath, in a letter to Francis Bacon[54]

In George R. R. Martin's novel series, A Song of Ice and Fire, Lord Wyman Manderly is mockingly called "Lord Lamprey" by his subjects in reference to his rumored affinity to lamprey pie and his striking obesity.[55]

Species

References

  1. ↑ Froese, Rainer, and Daniel Pauly, eds. (2009). "Petromyzontiformes" in FishBase. January 2009 version.
  2. ↑ Fossilworks: Order Petromyzontiforme
  3. ↑ "lamprey". Oxford University Press. Retrieved 12 February 2014.
  4. ↑ DOCKER, Margaret F (2006). "Bill Beamish's Contributions to Lamprey Research and Recent Advances in the Field.". Guelph Ichthyology Reviews. 7. Retrieved 12 June 2014.
  5. ↑ Hardisty, M. W.; Potter, I. C. (1971). Hardisty, M. W.; Potter, I. C., eds. The Biology of Lampreys (1 ed.). Academic Press. ISBN 9780123248015.
  6. ↑ Gill, Howard S.; Renaud, Claude B.; Chapleau, François; Mayden, Richard L.; Potter, Ian C.; Douglas, M. E. "Phylogeny of Living Parasitic Lampreys (Petromyzontiformes) Based on Morphological Data". Copeia. 2003 (4): 687–703. doi:10.1643/IA02-085.1.
  7. ↑ "CANADA: A Surfeit of Lampreys". Time. 9 May 1955. Retrieved 7 June 2008.
  8. ↑ Liem, Karel F.; William E. Bemis; Warren F. Walker, Jr.; Lance Grande (2001). Functional Anatomy of the Vertebrates. The United States of America: Thomson: Brooks/Cole. p. 50. ISBN 0-03-022369-5.
  9. 1 2 Haaramo, Mikko (11 March 2008). "Mikko's Phylogeny Archive". Retrieved 26 January 2009.
  10. ↑ Alaska Department of Fish and Game (2004). "Lampreys" (PDF). Retrieved 8 July 2012.
  11. ↑ The Dissection of Vertebrates: A Laboratory Manual
  12. ↑ Pancer, Z.; Amemiya, C. T.; Ehrhardt, G. T. R. A.; Ceitlin, J.; Gartland, G.; Cooper, M. D. (2004). "Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey". Nature. 430 (6996): 174–180. doi:10.1038/nature02740. PMID 15241406.
  13. ↑ Nagawa, Fumikiyo; Kishishita, Natsuko; Shimizu, Kazumichi; Hirose, Satoshi; Miyoshi, Masato; Nezu, Junnya; Nishimura, Toshinobu; Nishizumi, Hirofumi; Takahashi, Yoshimasa; et al. (2007). "Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice". Nature Immunology. 8 (2): 206–13. doi:10.1038/ni1419. PMID 17187071.
  14. ↑ Froese, Rainer, and Daniel Pauly, eds. (2011). "Petromyzontidae" in FishBase. February 2011 version.
  15. ↑ Macey, D. J.; Cake, M. H.; Potter, I. C. (1988). "Exceptional iron concentrations in larval lampreys (Geotria australis) and the activities of superoxide radical detoxifying enzymes". Biochemical Journal. 252 (1): 167–172. PMC 1149120Freely accessible. PMID 3421899.
  16. ↑ Derjean, D; Moussaddy, A; Atallah, E; St-Pierre, M; Auclair, F; Chang, S; Dubuc, R (2010). "A novel neural substrate for the transformation of olfactory inputs into motor output". PLOS Biology. 8 (12): e1000567. doi:10.1371/journal.pbio.1000567.
  17. ↑ Grillner, S. (2003). "The motor infrastructure: From ion channels to neuronal networks". Nature Reviews Neuroscience. 4 (7): 573–586. doi:10.1038/nrn1137. PMID 12838332.
  18. ↑ Saitoh, K.; Ménard, A.; Grillner, S. (2007). "Tectal Control of Locomotion, Steering, and Eye Movements in Lamprey". Journal of Neurophysiology. 97 (4): 3093–3108. doi:10.1152/jn.00639.2006. PMID 17303814.
  19. ↑ Brodin, L.; Shupliakov, O. (2006). "Giant reticulospinal synapse in lamprey: Molecular links between active and periactive zones". Cell and Tissue Research. 326 (2): 301–310. doi:10.1007/s00441-006-0216-2. PMID 16786368.
  20. ↑ In swimming, jellyfish and lampreys really pull their weight
  21. 1 2 Silva, S.; Araújo, M. J.; Bao, M.; Mucientes, G.; Cobo, F. (2014). "The haematophagous feeding stage of anadromous populations of sea lamprey Petromyzon marinus: low host selectivity and wide range of habitats". Hydrobiologia. 734 (1): 187–199. doi:10.1007/s10750-014-1879-4.
  22. ↑ "Prehistoric bloodsucker in Thames". BBC News. 1 July 2009. Retrieved 27 September 2012.
  23. ↑ "Giant blood sucker found in River Wear". The Northern Echo. 25 June 2009.
  24. ↑ Lehman, Don. "Chemical concerns may halt Lake Champlain treatments". poststar.com. The Post Star.
  25. ↑ Evans, Thomas M. (2012). Assessing Food and Nutritional Resources of Native and Invasive Lamprey Larvae Using Natural Abundance Isotopes. Thesis. Ohio State University.
  26. ↑ Silva, S.; Servia, M. J.; Vieira-Lanero, R.; Cobo, F. (2013). "Downstream migration and hematophagous feeding of newly metamorphosed sea lampreys (Petromyzon marinus Linnaeus, 1758)". Hydrobiologia. 700: 277–286. doi:10.1007/s10750-012-1237-3.
  27. ↑ Beamish, F. W. H. (1980). "Biology of the North American anadromous sea lamprey, Petromyzon marinus". Canadian Journal of Fisheries and Aquatic Sciences. 37: 1924–1943. doi:10.1139/f80-233.
  28. ↑ Nichols, O. C.; Tscherter, U. T. (2011). "Feeding of sea lampreys Petromyzon marinus on minke whales Balaenoptera acutorostrata in the St Lawrence Estuary". Journal of Fish Biology. 78: 338–343. doi:10.1111/j.1095-8649.2010.02842.x.
  29. ↑ Silva, S.; Servia, M. J.; Vieira-Lanero, R.; Nachón, D. J.; Cobo, F. (2013). "Haematophagous feeding of newly metamorphosed European sea lampreys Petromyzon marinus on strictly freshwater species". Journal of Fish Biology. 82: 1739–1745. doi:10.1111/jfb.12100.
  30. 1 2 Nelson, J. S. (2006). Fishes of the World (4th ed.). New York: John Wiley and Sons, Inc. pp. 601 pp. ISBN 0-471-25031-7.
  31. ↑ Forey, Peter; Janvier, Philippe (2000). "Agnathans and the origin of jawed vertebrates". In Gee, Henry. Shaking the tree: readings from Nature in the history of life. USA: University of Chicago Press; Nature/Macmillan Magazines. pp. 251–266. ISBN 978-0-226-28497-2.
  32. ↑ Janvier, P. (2008). "Early Jawless Vertebrates and Cyclostome Origins". Zoological Science. 25 (10): 1045–1056. doi:10.2108/zsj.25.1045. PMID 19267641.
  33. ↑ Haaramo, Mikko (2003). "Petromyzontidae – lampreys". in Mikko's Phylogeny Archive. Retrieved 25 November 2013.
  34. ↑ Froese, Rainer, and Daniel Pauly, eds. (2012). "Petromyzontiformes" in FishBase. April 2012 version.
  35. ↑ Chang, M. M.; Zhang, J.; Miao, D. (2006). "A lamprey from the Cretaceous Jehol biota of China". Nature. 441 (7096): 972–974. doi:10.1038/nature04730. PMID 16791193.
  36. ↑ "Discovery of the Oldest Fossil Lamprey in the World". University of the Witwatersrand. 26 October 2006. Archived from the original on 16 March 2008. Retrieved 8 June 2008.
  37. ↑ "Scientists find lamprey a 'living fossil'". University of Chicago Medicine. 26 October 2006.
  38. ↑ Gess, R. W.; Coates, M. I.; Rubidge, B. S. (2006). "A lamprey from the Devonian period of South Africa". Nature. 443 (7114): 981–984. doi:10.1038/nature05150. PMID 17066033.
  39. ↑ Araújo, M.J., Silva, S., Stratoudakis, Y., Gonçalves, M., Lopez, R., Carneiro, M., Martins, R., Cobo, F. and Antunes, C. 2016. Sea lamprey fisheries in the Iberian Peninsula, pp.115-148. In Jawless Fishes of the World. Volume 2, Chapter: 20. Ed. by A. Orlov and R. Beamish. Cambridge Schoolars Publishing
  40. ↑ Judith A. Green, 2006, Henry I: King of England and Duke of Normandy, p. 1, Cambridge, CAM, GBR:Cambridge University Press, ISBN 0521591317, see , accessed 1 July 2015.
  41. ↑ "Gloucester lamprey pie is fit for the Queen". BBC News. 20 April 2012.
  42. ↑ Froese, Rainer and Pauly, Daniel, eds. (2012). "Lampetra fluviatilis" in FishBase. September 2012 version. (citing Bristow, Pamela (30 April 1992). The Illustrated Encyclopedia of Fishes. London: Chancellor Press. ISBN 9781851521364.).
  43. ↑ Deshpande, S. S. (29 August 2002). Handbook of Food Toxicology. CRC Press. p. 695. ISBN 978-0824707606.
  44. 1 2 Gunn, edited by J.M.; Steedman,, R.J.; Ryder, R.A. (2003). Boreal Shield Watersheds Lake Trout Ecosystems in a. London: CRC Press. p. 40. ISBN 9780203495087. Retrieved 8 November 2015.
  45. ↑ Alexander, Jeff (2009). Pandora's locks the opening of the Great Lakes-St. Lawrence Seaway. East Lansing, Mich.: Michigan State University Press. ISBN 9781609171971. Retrieved 8 November 2015.
  46. ↑ Williams, Ted (2007). Something's Fishy an Angler's Look at Our Distressed Gamefish and Their Waters – And How We Can Preserve Both. New York: Skyhorse Publishing, Inc. p. 382. ISBN 9781628731972. Retrieved 8 November 2015.
  47. ↑ O'Sullivan, edited by P.E.; Reynolds, C.S. (2007). The Lakes Handbook, Volume 2. Oxford: John Wiley & Sons. p. 81. ISBN 9781405141109. Retrieved 8 November 2015.
  48. ↑ Peter W. Sorensen, 2015, "Applications of pheromones in invasive fish control and fishery conservation (Ch. 12)," in Fish Pheromones and Related Cues (P.W. Sorensen & B.D. Wisenden, Eds.), pp. 255–268, ISBN 978-0813823867, Hoboken, NJ, USA:Wiley-Blackwell, see and , accessed 1 July 2015.
  49. ↑ P.W. Sorensen & T. R. Hoye, 2007, "A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus," J. Fish Biol. 71(Supplement): pp. 100–114, see , accessed 1 July 2015.
  50. ↑ Mary L. Moser, Pedro R. Almeida, Paul S. Kemp & P.W. Sorensen, 2014, "Lamprey spawning migration (Ch. 5, §5.6.1, Pheromones)," in Lampreys: Biology, Conservation and Control, Vol. 1 (Margaret F. Docker, Ed., Vol. 37, Fish & Fisheries Series), Berlin, BE, DEU:Springer, ISBN 9401793069, see , accessed 1 July 2015.
  51. ↑ Entry in Grimm's German Dictionary, online edition at Trier University
  52. ↑ Seneca the Younger. L. ANNAEI SENECAE AD NOVATVM DE IRA LIBER III [On Anger] (in Latin). III. Thelatinlibrary.com.
  53. ↑ Plutarch. The Morals. V. William W. Goodwin. Online Library of Liberty. Translated by William Watson Goodwin.
  54. ↑ von Hofmannsthal, Hugo (1902). "The Letter of Lord Chandos".
  55. ↑ Martin, George R. R. (16 November 1998). A Clash of Kings (1 ed.). Voyager Books. ISBN 0-00-224585-X.

Further reading

General

Pest management

Examples of research on pheromone function and use

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