Petromyzon marinus, sea lamprey

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Phylogeny

The phylum Chordata (chordates) includes three major taxa: Cephalochordata, represented by lancelets; Tunicata (also Urochordata), represented by ascidians; and Craniata.

Under some phylogenies, Craniata consists of two taxa: Vertebrata (vertebrates) that contains Gnathostomata (gnathostomes or jawed vertebrates) and their sister group Hyperoartia (petromyzontids or lampreys), and Hyperotreti (myxonids or hagfishes). Under this scheme, hagfishes are the sister group to the vertebrates. However, lampreys and hagfishes do share unique features and some phylogenies unite the two groups as Agnathans or Cyclostomes within the vertebrates. Under both scenarios, some features shared by lampreys and gnathostomes may represent primitive conditions at the level of the vertebrates, which makes lampreys of considerable interest to vertebrate evolutionary biologists.

The phylogenetic relationships between the three groups of Craniates - lampreys, hagfishes and gnatostomes - are still not completely resolved. Fossil and molecular data suggest that cyclostomes diverged from gnatostomes about 535 to 462 million years ago.

From an ecological perspective, adult lampreys use three feeding strategies: anandromous lampreys (two species P. marinus and L. japonica), freshwater parasitic lampreys (spend entire life in freshwater streams and rivers), and brook lampreys (about 20 species of dwarf lampreys nonparasitic in adulthood).

Buccal glands of parasitic lampreys produce substance lamphedrin that consists of two proteins with anticoagulant and lytic properties.

Parasitic lampreys can be divided into two groups: blood feeding (P. marinus and Mordacia species) and flesh feeding (such as Lampetra fluviatitis and Geotria australis). On the basis of recent cladistic analysis, blood-feeding is ancestral to flesh feeding in Petromyzontidae. The brook lampreys most likely evolved from parasitic freshwater ancestors by delaying metamorphosis and shortening the adult stage.

Taxonomy of lampreys

Linnaeus first described the sea lamprey, Petromyzon marinus, in 1758 ("myzon" means "sucker" in Greek). There are about 40 species of lamprey in the family Petromyzontidae divided among 8 genera: Entosphenus, Eudontomyzon, Geotria, Ichthyomyzon, Lampetra, Lethenteron, Mordacia, Petromyzon. Lampreys are considered taxonomically to be among the most primitive of living vertebrates.

Taxonomic lineage

cellular organisms - Eukaryota - Fungi/Metazoa group - Metazoa - Eumetazoa - Bilateria - Coelomata - Deuterostomia - Chordata - Craniata - Vertebrata - Hyperoartia - Petromyzontiformes - Petromyzontidae - Petromyzon - Petromyzon marinus

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Brief facts

Worldwide distribution

The sea lamprey, Petromyzon marinus, is a fish native to coastal North Atlantic watersheds. Historically it is found on both sides of the Atlantic Ocean and ranges from northern Norway along the western European coast to the Mediterranean Sea, including the Baltic and the offshore islands of the Faroes and the British Isles. The North American distribution is discontinuous: there are sea lampreys on the southwest coast of Greenland and then a gap in the population until the coast of Labrador. They then are found along the Atlantic coast to northern Florida and the Gulf of Mexico.

Anandromous and landlocked lamprey

It is important to recognize existence of two populations of North American sea lamprey:

• Anandromous sea lamprey is a native component of North Atlantic aquatic ecosystems. Adult sea lampreys spend 1.5-2 years in the ocean, where they grow to maturity, after which they return to freshwater rivers and streams for spawning. The anandromous sea lampreys cannot survive in fresh water as adults. They do not parasitize on fish while in fresh water (temporary attachment without active feeding sometimes is observed) and do not affect population of native fresh water species.
• Landlocked sea lamprey is a self-sustained population of the lampreys adapted to complete their whole life cycle in fresh water in the upper Great Lakes. Parasitic activities of landlocked lamprey have a great impact on many valuable fish species native to Great Lakes and, at some point, led to collapse of many commercial fisheries. Landlocked form of lamprey, native to Lake Ontario, gained access to the upper Great Lakes after construction of the Welland Ship Canal that was built in 1829 to pass ocean-going ships around Niagara Falls. The first lamprey spawning was reported in tributaries to Lake Eerie in 1932. It never become abundant in Lake Eerie but invaded the rest of the upper Great Lakes by the end of 1940's. It is still not clear what genetic modifications enabled sea lamprey to adapt in living in freshwater because captive anandromous lamprey held in the fresh water do not survive longer than several months and die even when given access to appropriate hosts.

Lampreys native to the upper Great Lakes

Five species of the family Petromyzonidae are resident to the upper Great Lakes (lakes Superior, Michigan, and Huron and their tributary system), four of which are native to the lakes' ecosystem.

• Lampetra lamotteni (American brook lamprey) - adult stage is not feeding
• Ichthyomyzon castaneus (chestnut lamprey) - parasitic at adult stage
• Ichthyomyzon fossor (northern brook lamprey) - adult stage is not feeding
• Ichthyomyzon unicuspis (silver lamprey) - parasitic at adult stage

General description of adult P. marinus

The adult sea lamprey has an elongated body 720-880 mm in length. It has no ribs, no paired fins, no jaws (Agnatha), and has seven pairs of gill pouches. Lampreys belong to vertebrates because they have cartilaginous skeletal structures in the form of vertebral arches that protect the spinal cord.

One of the most distinguishing external characteristics of the adult sea lamprey it is its mouth (sucker) that contains 11 or 12 rows of teeth, arranged in concentric circles enclosed by an oral hood. The teeth-hood arrangement is also called buccal funnel or suctorial disk. With help of the sucker, the lamprey fastens itself to various objects. There are two main types of behaviors associated with using of the sucker:

• Feeding is what adult lampreys do in the ocean when they rasp a hole in the side of their host (prey), burrow their buccal funnel under the skin and feed on the host's fluids
• Attachment is the non-feeding act of holding on to another fish or object in order to rest from swimming during migration or to catch a ride on another ocean-bound fish or object (usually used by transformers).

Role of anandromous P. marinus in freshwater ecosystem

• Sea lamprey spawning activities restore and enhance streambed structure that benefits many other species. Some fish species such as minnows, common shiners, fallfish, and salmonids use sea lamprey nests for their own spawning activities such as redd building sites and as refugia for fry. Cleaning and loosening of substrate improves movement of oxygen-rich water through microhabitats of many aquatic organisms such as insect larvae, crayfish, tadpoles, fish larvae, etc.
• Freshwater fish that prey upon sea lamprey include brown trout, northern pike and walleye.
• During migrations and spawning, sea lamprey adults are vulnerable to predation by bitterns, hawks, herons, gulls, osprey, and owls, muskrats, otters, raccoons, weasels, foxes, and water snakes.
• Sea lamprey transformers can sometimes attach to freshwater fish. This is usually happens when the transformers had to overwinter in freshwater. Usually no active feeding occurs and all fish survives with barely a broken skin.

Role of anandromous P. marinus in ocean ecosystem

• Sea lamprey parasitize on a long list of marine species including alewives, blueback herring, American eel, American shad, sturgeon, Atlantic cod, Atlantic herring, Atlantic mackerel, Atlantic menhaden, Atlantic salmon, basking shark, bluefin tuna, bluefish, haddock, hake, swordfish, weakfish, pollock, sei whale.
• Marine fish that have been documented to prey upon sea lamprey include Atlantic cod, swordfish, striped bass and other sea lamprey.

Control of landlocked sea lamprey

• Lampricides 3-trifluoromethyl-4-nitrophenol (TFM), occasionally in conjunction with 2-amino-ethanol salt of 2'5-dichloro-4'-nitrosalicylanilide (Bayer 73), are used to kill larval sea lampreys in streams.
• Capture and sterilization of mature (spermiated) males by injecting them with P,P-bis(aziridin-1-yl)-N-methylphosphinothioic amid (biazir) and re-introduction them into spawning locations where they compete with intact males thus reducing quantities of fertilized eggs.
• Use of migratory and sex pheromones to attract and then, in some instances, trap sea lampreys. Advantages of pheromones include potency, easy and inexpensive production and environmental safety.

Pheromones of sea lampreys

Sea lamprey produces at least two types of chemoattractants: sexual (produced by spermiating males to attract mature females) and migratory (produced by sea lamprey larvae).

Sea lamprey is an anandromous species; however, studies have demonstrated that sea lampreys do not home to their natal streams. Instead they choose specific streams that have large numbers of larvae. Sea lampreys are not good swimmers and may be transported by their hosts great distances. This strategy of using pheromones is advantageous for the species in finding appropriate spawning and nursery habitat.

A unique sea lamprey bile acid, petromyzonol sulfate (PS) (disulfated aminosterol derivative, petromyzonamine disulfate (PADS)) and its two precursors were found to exert strong and highly specific olfactory effect on the sea lamprey olfactory system. Larval odor is very potent attractant to migratory sea lamprey: 1 g larva may activate well over 300 liters of river water in 1 hour.

Interestingly, this compound also shows structural similarity to squalamine, a unique antimicrobial agent discovered in sharks.

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Life cycle of anandromous Sea Lamprey

These anandromous species has a full life span of 8-11 years.

• unfertilized egg Ovulation of eggs into coelom (Piavis stage 0)
• embryo The embryonic development in the eggs takes about 10-13 days. The eggs can survive and develop successfully in very narrow range of temperatures. The temperature of 18.4 °C was determined to be optimum for development of the sea lamprey. Embryos develop abnormally and often arrest in development at temperatures even slightly below the optimum. The duration of embryological stages is usually considered as the time interval between the first appearance of a stage and the earliest appearance of the following stage.
  • zygote Fertilization, approx. duration 2 hr. (Piavis stage 1)
  • 2 cells 1^st cleavage furrow, approx. duration 6 hr. (Piavis stage 2)
  • 4 cells 2^nd cleavage furrow, approx. duration 2-3 hr. (Piavis stage 3)
  • 8 cells 3^rd cleavage furrow, approx. duration 3-5 hr. (Piavis stage 4)
  • 16 cells 4^th cleavage furrow, approx. duration 3 hr. (Piavis stage 5)
  • 32 cells More than 16 cells, approx. duration 3 hr. (Piavis stage 6)
  • 64 cells More than 32 cells, approx. duration 5 hr. (Piavis stage 7)
  • blastula More than 64 cells, approx. duration 40 hr. (Piavis stage 8)
  • gastrula Appearance of blastopore, approx. duration 32-40 hr. (Piavis stage 9)
  • neural plate
    and groove Flattening of dorsal region of embryo from blastopore to anterior extremity, approx. duration 24 hr. (Piavis stage 10)
  • Neural rod Mid-dorsal union of neural folds, approx. duration 24 hr., approx. duration 48-96 hr. (Piavis stage 11)
  • Head Raising anterior portion of embryo above yolk mass, the head and "neck" region curves toward the posterioventral portion, approx. duration 48 hr. (Piavis stage 12)
  • Prehatching Muscular activity in head region, approx. duration 48-96 hr. (Piavis stage 13)
  • hatching Rupture of fertilization membrane, approx. duration 64 hr. Heart begins beating. (Piavis stage 14)
• pro-larva After eggs hatched, lampreys stay in the nest for 4-5 days during which they develop gills, pigmentation and buccal hood.
  • pigmentation Appearance of melanophores, approx. duration 48-64 hr. (Piavis stage 15).
  • gill cleft Appearance of gill slits and velum beat, approx. duration 48 hr. (Piavis stage 16).
  • burrowing prolarva Appearance of bilateral eyespots, posterior progression of transparency as the gut differentiates, and burrowing ability (Piavis stage 17). The burrowing prolarvae were produced only within relatively narrow range of 15.5-21.1 °C (Piavis, 1961).
  • larva Opening of lumen of yolk-filled gut and differentiation of all systems except genital (Piavis stage 18).
• ammocoete ['amə'sēt] Larvae drift downstream where they burrow into the muddy bottoms of the streams, rivers and lakes where they stay for 4-8 years filter-feeding upon planctonic microorganisms. The larva is about 6 inches long and resembles lancelet. There is a reliable method of determining the age of the larval lamprey by statoliths. Statoliths display an alternating narrow opaque band that represents slow growth during winter, with translucent band that formed during rapid growth at increased temperatures and feeding in summer time.
• metamorphosis
  MeSH After being in larval stage for 5-7 years, lampreys undergo a radical metamorphosis which involves a drastic re-arrangement of internal organs, development of eyes and transformation from mud-dwelling filter feeder into efficient swimming predator/parasite; the metamorphosis is spontaneously initiated or inhibited depending upon the coordination of a complex integration of environmental, metabolic and hormonal cues, when the size (length and weight), condition factors, and lipid stores reach appropriate levels and coincide with the post-winter rise in water temperature. Metamorphosis lasts for four to six months.
• macrophthalmia Newly metamorphosed lamprey commonly referred to as transformers. Transformers are about 6-10 inches long. They typically do not linger in the fresh water. In fall, typically between September and December, Maine lampreys migrate downstream to sea. Low water flows or other obstructions (for example, dams) may delay migration until the following spring. Transformers are the only stage in the life cycle of anandromous lamprey that may attach to, and possibly feed upon other fish in freshwater. However freshwater feeding by juvenile sea lamprey has minimal or no negative impact on populations of native or sport fisheries. Great Lakes seq lamprey juveniles move downstream to the Great Lakes, where they quickly find fish on which to feed and their next, parasitic life stage begins
• adult
  • parasitic stage Adult lampreys are obligatory parasites of other fish during 18-20 months maturing at sea. The lamprey fastens onto a fish and digs out a hole in its side; the saliva keeps the wound open for hours or weeks, until the lamprey let go or the fish dies. Parasitism usually does not involve killing the host, however, sometimes, depending on size and physical conditions of both parties, host dies from the wound(s) and secondary infections. The sea lamprey can parasitize on many marine fish species including other lampreys. Adult lampreys grow 18-24 inches in length and weight from 0.8 to 1.4 kg.
  • migration Adult sea lamprey may migrate hundreds of kilometers upstream to find suitable spawning habitat. They use their specialized mouths to hold onto rocks or other objects to assist them in overcoming obstacles. When they enter freshwater, they stop feeding.
  • spawning Spawning season varies longitudinally and usually peaks when water temperature reach optimum range about 17-19 °C (for example, in Maine, spawning occurs from late May through early summer). Males and females work together to construct elongated nests of gravel and small rocks, which they often carry in their mouths. The nests are 25 to 50 cm deep and up to a meter long. They clean nests from silt by undulating motions of their bodies. Each female will produce an average of 230,000 tiny white adhesive, non-buoyant eggs 1.0-1.4 mm in diameter. The bodies of spawned lampreys deteriorate rapidly, and they die.

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Lampreys attached to the trout

Sea lamprey's sucker

Scott Fields. Great Lakes Resource at Risk Environ Health Perspect. 2005 March; 113(3): A164–A173.

A sticky situation. The sea lamprey, a non-native species that probably swam into the Great Lakes from the Hudson River, attaches to lake trout and whitefish (above). Sea lampreys have invaded all the Great Lakes and wiped out fisheries.

References

• Richardson MK, Wright GM. Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus). J Morphol. 2003 Sep;257(3):348-63. PMID: 12833373
• Hoye TR et al. Details of the structure determination of the sulfated steroids PSDS and PADS: new components of the sea lamprey (petromyzon marinus) migratory pheromone. J Org Chem. 2007 Sep 28;72(20):7544-50. PMID: 17718505
• Venkatachalam KV. Petromyzonol sulfate and its derivatives: the chemoattractants of the sea lamprey. Bioessays. 2005 Feb;27(2):222-8. PMID: 15666352
• Renaud CB et al. Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lamprey. Journal of Zoology, Volume 278, Number 3, July 2009 , pp. 231-242(12)
• Allen J. Smith, John H. Howell and George W. Piavis, 1968 Comparative Embryology of Five Species of Lampreys of the Upper Great Lakes
• Nikitina N et al. The Sea Lamprey Petromyzon marinus: A Model for Evolutionary and Developmental Biology. Cold Spring Harb. Protoc.; 2009; doi:10.1101/pdb.emo113.
• Osório J, Rétaux S. The lamprey in evolutionary studies. Dev Genes Evol. 2008 May;218(5):221-35. PMID: 18274775
• Dittman A. Chemical cues for sea lamprey migration. Nat Chem Biol. 2005 Nov;1(6):316-7. PMID: 16408065
• Sea Lamprey. Petromyzon marinus Linnaeus 1758. Prepared by Kircheis FW. (2004)
• Major topic "salmon": free full-text articles in PubMed
• Quintella, B. R., Andrade, N. O. & Almeida, P. R. 2003 Distribution, larval stage duration and growth of the sea lamprey ammocoetes, Petromyzon marinus L., in a highly modified river basin. Ecol. Freshw. Fish 12, 286–293. (doi:10.1046/j.1600-0633.2002.00030.x)