Ctenophora

Comb jellies
"Ctenophorae" from Ernst Haeckel's Kunstformen der Natur, 1904
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Ctenophora Eschscholtz, 1829
Classes
Tentaculata Nuda

The phylum Ctenophora, commonly known as ctenophores or comb jellies, is a phylum classically grouped with Cnidaria in the Coelenterata infrakingdom. The phylum includes the sea gooseberry (Pleurobrachia pileus) and Venus' girdle (Cestum veneris). The word ctenophore (pronounced without the c, /tiːn.ou.fɔː(ɹ)/) comes from Greek, kteno-, kteis, "comb" and -phore, meaning "bearer". It comes via the New Latin ctenophorus in the 19th century.

Despite their appearance, they are zoologically not true jellyfish, not least because they lack the characteristic cnidocytes. There are more than 100 varieties of ctenophore spread throughout the world's oceans, which form a considerable proportion of the entire plankton biomass. A few species, such as the sea gooseberry, native to the North Sea, have reached such high populations that they clog fishermen's nets, while of other species only a few examples are known. The fragile makeup of ctenophora makes research into their way of life extremely difficult; for this reason data on their lifespan are not available, but it is known that ctenophora begin to reproduce at an early age and so can be assumed to have a short generation cycle.

Anatomy and morphology

Body

Light refracting off a Mertensia ovum

Ctenophora are generally colourless, but they can have red, orange, or even black colour in certain species. The most common species are often only a few centimetres long. The exceptions are the species of the genus Cestum, which can reach up to one and a half metres.

The species which live in deep waters, such as the red tortuga, can appear brightly-coloured, although usually with pigments that absorb blue light, making them appear dark in the sea. A deep-sea species informally called the “Tortugas Red” is bright red in colour, presumably to absorb blue-light from its prey and the environment. Like many other ctenophores, can give off light by means of bioluminescence. One species, Eurhamphaea vexilligera, can give off an exudate of red ink which glows blue in the dark, perhaps to dissuade predators.

Ctenophora have an interesting form of symmetry, with many bilateral components, but a few asymmetrical structures such as the anal pores near the statocyst and sometimes the proportions of their auricles (ciliated lobe-like structures).

Ctenophorans are diploblastic (having only two body layers). The body consists of two transparent cell layers, which make up its outer skin (ectoderm) and inner skin (gastroderm). The ectoderm, made up of two cell layers, is mostly covered by a protective layer of slime, excreted by special glands. The gastroderm surrounds a cavity which serves as a stomach and is only accessible by the mouth opening, connected by a long, narrow gullet. Captured quarry is pre-digested in the gullet by strong enzymes and fully decomposed in the stomach. There is no separate exit from the stomach apart from two 'anal pores', which despite their name appear to be only moderately used for excretion, so indigestible waste is principally expelled via the mouth.

The space between the inner and outer skin is taken up by the mesoglea, a thick, transparent, jelly-like layer made from collagen and connective tissue, pervaded by numerous small canals, which are used for transport and storage of nutrients. The position of the canals varies from species to species, but they mostly run directly underneath the tissues that they serve. The extracellular net of structural protein is kept upright by special cells similar to amoebas.

The mesogloea may also play a role in the lift of the creatures. Cilia found in the canals of the digestive system may serve to pump water in or out of the mesogloea, when osmotic water pressure changes, perhaps because the creature has swum out of saline sea water into coastal brackish water. Ctenophora do not possess a specific circulatory system, neither do they have any organs for breathing; gas exchange and the excretion of waste products of cell metabolism such as ammonia occur over the body's entire surface through simple diffusion. The body is pervaded by a simple net of neurons without a 'brain'. These nerves are concentrated around the mouth, tentacles, 'combs' and statocysts and are connected with the muscular cells found in the mesogloea and the inner cellular layer of the ectoderm.

Statocysts

Undescribed deep-sea species with tentacles and clearly visible side-branches (tentilla)

The statocyst is a specialised system of the ctenophore that serves as a balancing organ and also controls its movement. It can be found on the end of the body opposite the oral opening and is formed by a collection of a few hundred calcareous cells balanced on four horizontal groups of serpentine flagella, known as the statolith. As outside influences cause the ctenophore to change its position, the statolith puts more pressure on one of the four flagella groups than on the other three. This sensation is transmitted to the ectoderm, which is propagated along eight long "comb rows" (ctenes). The ctenes are formed from rows of cilia, which coalesce with one another in groups of hundreds and form ctenes or comb plates about 2-5 millimetres long. By erecting these ctenes in succession, the ctenophore can use them as an oar, which, when the eight ctenes are properly synchronised, allow it to propel itself through the water. A ciliary group of the statocyst is needed for every quadrant and controls two ctenes as a pacemaker. The rhythm is carried automatically, and the signal is propagated mechanically, and not by nerve impulses.

Whether gravity acting on the statocyst raises or lowers the stroke frequency depends on the "disposition" or geotaxis of the ctenophore; the ctenophore can alter the beat frequency of different comb rows to either swim upward or downward in the water column. The "disposition" of the ctenophore is determined by sensations handled by the nerve net, in association with the ambient light levels.

Tentacles

Many species have two opposing retractable tentacles emerging somewhere near the midpoint of the body, which are used to catch prey. From these central tentacles branch additional filaments called tentilla, which unlike in Cnidaria do not contain stinging cells, but colloblasts or "lasso cells". These cells burst open when prey comes in contact with the tentacle. Sticky threads released from each of the colloblasts will then capture the food. The colloblasts, like the tentacle, are regularly fully regenerated.

Not all varieties rely mainly on tentacles. Some like Beroe engulf gelatinous prey directly, and others instead use their muscular mouth lobes to catch food, with oral tentacles serving a secondary entangling function.

Regeneration

Ctenophora are capable of extraordinary regeneration; even if half of the creature is destroyed, often the remaining half can rebuild itself. The same is true of single organs such as the statoliths, which can be regenerated even after being completely lost.

Movement

Many Ctenophora simply let themselves drift with the current. They can however also swim, sometimes quite rapidly, by means of the strokes of their cilia. They are the largest animal to use their cilia for movement and can reach speeds of about five centimetres a second. A possible evolutionary advantage is that constant strokes do not cause vibrations that would alert prey or predators.

Some varieties also flap their oral lobes during escape swimming, while others move by undulating their body or creeping like flatworms.

Distribution

As an invasive species

Although ctenophores are generally hardly noticeable and their influence on an ecosystem is ostensibly very low, they can still do significant damage when they occur in non-native waters. The North Atlantic species Mnemiopsis leidyi was brought by ships' ballast water into the Black Sea and spread rapidly. Within ten years the anchovy fishing industry around the sea had collapsed, as the newly introduced species fed on the same plankton as the anchovy larvae. The biomass of ctenophora in the Black Sea reached a million tons at the highest point of its development.

Through the similarly sudden appearance in 1997 of another ctenophore, Beroe ovata, which feeds on Mnemiopsis leidyi, the balance was somewhat restored; since then the Black Sea has been occupied by both foreign species. The same scenario with the same species has now begun to be played out in the Caspian Sea, and Mnemiopsis was also reported from the North Sea in 2006.

Ecology and life history

Habitat

All Ctenophora live in the sea, where they live in depths of up to four kilometres. As plankton they are largely subject to movement of ocean currents, although various species are particular to certain habitats. They can be found in abundance in the tropic and to the both poles.

The most well-known species live as plankton in the ocean layers near the surface. However, as they are largely transparent, extremely fragile and rarely grow longer than a few centimetres, they are unknown to most people. On the coast Pleurobrachia species (called sea gooseberries) are encountered most frequently by beachgoers. Bolinopsis, Mnemiopsis and the tentacle-less Beroe can also be found fairly frequently.

About 35 species live on the sea bed. These species are ordered in the taxon of platyctenidae, due to their flattened forms which more closely resemble slugs or flatworms than jellyfish.

The ctenophore Mertensia ovum is one of the most predominant members of plankton in arctic waters.

Community Ecology

A ctenophore (Beroe sp.) looking for food. The mouth is on the left.

Ctenophora are predators which use their tentacles to catch plankton, larvae, worms, crustaceans, Cnidaria, other Ctenophora, and sometimes small fish. When their tentacles are loaded with food, they can be retracted and wiped off. The food is then carried into the stomach either by mucus or inner cilia. The species of the genus Haeckelia feed almost exclusively on cnidaria, but do not digest their cnidocytes; instead they build them into their own tentacles as 'kleptocnidae'. This 'theft' baffled zoologists for a long time as they falsely assumed ctenophora were also capable of forming cnidocytes. Parasitism has only been observed in a single genus, Lampea, which is parasitic on salps when too small to engulf them entirely.

Among the species that prey on ctenophora are cnidaria, sea turtles, various fish such as mackerels and lumpfish, seabirds and other ctenophora.

Life History

Larva of Bolinopsis sp.

Ctenophora reproduce sexually, with the exception of some species of the order Platyctenida that reproduce asexually. Almost all ctenophores are hermaphroditic or monoecious, possessing both male and female reproductive organs, which lie directly under the 'combs' near the small channels of the mesogloea. The tropical lobate Ocyropsis is one genus with separate sexes. With almost all species, when triggered by outside lighting conditions, the gametes are discharged into the surrounding water through small openings in the ectoderm, the gonopores, where external fertilisation takes place. Self-fertilization is somewhat rare. The platyctene Tjalfiella tristoma, is viviparous; that is, the young grow in a brood chamber.

Certain species of Ctenophores, like Beroe ovata, have a special method of preventing polyspermy. After several sperm pronuclei have entered the egg, the egg pronucleus goes through a process where it migrates around the cell and finally chooses which sperm pronucleus it wants to fuse with, rejecting others because of signals indicating close relationship or lack of fitness.

After the fertilised eggs have divided twice, the ctenophore's later radial body symmetry has already been set. They develop into a free-floating cydippid state, which looks very similar between all ctenophora and sometimes is labeled as a larva, although in many cases this already represents a miniature version of what the creature will grow up to be. Among some groups such as lobates and platyctenids, the cydippid and adult forms do differentiate morphologically, so that the 'larva' label is more appropriate.

Etymology and Taxonomic history

Early classification

Sailors have observed ctenophores since ancient times. However, the first recorded sighting only came in 1671, made by a ship's doctor. The Swedish taxonomist Carl von Linné classified them with other 'primitive' invertebrates such as sea sponges (Porifera) or cnidaria as 'zoophytes' ("animal plants"), alluding to the passive, "plant-like" character of the creatures. The French zoologist Georges Cuvier supported this classification. Only in the 19th century were ctenophora recognised as a standalone taxon.

Historical phylum

Bathocyroe fosteri a common but fragile deep-sea lobate, oriented mouth down

The initial classification of ctenophora has been disputed. According to cladistics, currently the leading ordering method, ctenophora are more closely related to the reflectively symmetrical bilateria than cnidaria. The fact that they have two opposing tentacles, breaking their radial symmetry and making them reflectively symmetrical, supports this, although certain structures give them a rotational or biradial symmetry. They differ from cnidaria in their possession of true muscle tissue, sticky colloblasts in place of cnidocytes, and their 'combs'. Another important sign of ctenophore's relationship with bilateria is the form of their spermatozoa. These consist in both groups of a single, large acrosome and a subacrosomic perforation disc. Cnidarian spermatozoa, in contrast, possess several acrosomic vesicles.

For this reason the 'classical' grouping of Coelenterata stands opposite the alternative taxon of acrosomata:

Alternative 1: Coelenterata

• Eumetazoa
  • Bilateria
  • Coelenterata
    • Cnidaria
    • Ctenophora

Alternative 2: Acrosomata

• Eumetazoa
  • Cnidaria
  • Acrosomata
    • Bilateria
    • Ctenophora

In addition it has been suggested that ctenophora have a close relationship with flatworms, due to the similarities between flatworms and the flattened ctenophora of the order Platyctenida are one of the justifications for this. Some zoologists consider this resemblance superficial, and not indicative of a close relationship.

The soft bodies of ctenophores, which have no hard parts whatsoever, makes fossilisation generally very improbable, meaning that the phylogeny of ctenophora fossils is very sparsely documented. The sole fossil records, of Archaeocydippida hunsrueckiana and Paleoctenophora brasseli, date from the Devonian Period; enough details remained in the fine-grained schist of Hunsrück to make identification possible. It is disputed whether the species Maotianoascus octonarius, known from the Chengjiang Fauna of the lower Cambrian Period, is a member of the ctenophore phylum, while three species, Ctenorhabdotus capulus, Fasciculus vesanus and Xanioascus canadensis, are known from the Cambrian Burgess Shale.

Classification

Currently about a hundred species are known, which are traditionally split into the classes of Tentaculata (also known as Tentaculifera) and Nuda (also known as Atentaculata).

• The Tentaculata make up by far the largest number of species; as their name implies, they possess tentacles, although these are sometimes vestigial. They are divided into the following six orders:
  • Cydippida, which includes the sea gooseberry (Pleurobrachia pileus)
  • Platyctenida
  • Ganeshida (probably larval form)
  • Thalassocalycida
  • Lobata
  • Cestida, which includes the Venus' belt (Cestum veneris)
• The Nuda class contains only a single order, Beroida, to which the melon jelly (Beroe gracilis) belongs. As again the name of the taxon implies, they are distinguished by the complete absence of tentacles.

Due to the continued uncertainty over the ordering of ctenophora it is currently unclear whether the above divisions correctly reflect the actual phylogeny of the taxon. Molecular genetic studies indicate that cydipidda is a polyphyletic group, i.e. it does not include all the descendents of their common ancestor, and so the overall classification of the group needs to be revised.

The following diagram shows the putative phylogeny of ctenophora on the basis of morphologic and molecular genetic data (RNA):

Ctenophora
|--Cydippida (Mertensiidae family)
|--
    |--Platyctenida
    |--
        |--Cydippida (Pleurobrachidae family)
        |--
        |   |--Nuda Beroida
        |   |--Cydippida (Haeckeliidae family)
        |
        |--
            |--Lobata
            |--Cestida
            |--Thalassocalycida

The above details are however still in doubt. For the time being the phylogeny of ctenophora must be regarded as unsettled.

Bibliography

• Much of this article is based on a translation of the corresponding German-language Wikipedia article, retrieved on 5 April 2006.

• D. T. Anderson, Invertebrate Zoology, 2nd ed, Oxford Univ. Press, 2001, Ch. 3, p. 54, ISBN 0-19-551368-1
• R. S. K. Barnes, P. Calow, P. J. W. Olive, D. W. Golding, J. I. Spicer, The invertebrates – a synthesis, 3rd ed, Blackwell, 2001, ch. 3.4.3, p. 63, ISBN 0-632-04761-5
• R. C. Brusca, G. J. Brusca, Invertebrates, 2nd Ed, Sinauer Associates, 2003, ch. 9, p. 269, ISBN 0-87893-097-3
• J. Moore, An Introduction to the Invertebrates, Cambridge Univ. Press, 2001, ch. 5.4, p. 65, ISBN 0-521-77914-6
• E. E. Ruppert, R. S. Fox, R. P. Barnes, Invertebrate Zoology – A functional evolutionary approach, Brooks/Cole 2004, ch. 8, p. 181, ISBN 0-03-025982-7
• W. Schäfer, Ctenophora, Rippenquallen, in W. Westheide and R. Rieger: Spezielle Zoologie Band 1, Gustav Fischer Verlag, Stuttgart 1996
• Bruno Wenzel, Glastiere des Meeres. Rippenquallen (Acnidaria), 1958, ISBN 3-7403-0189-9

Scientific literature

• Harbison, G. R. 1985. On the classification and evolution of the Ctenophora. pp 78-100 in The Origins and Relationships of Lower Invertebrates. (S. C. Morris, J. D. George, R. Gibson and H. M. Platt, eds.). Oxford University Press, Oxford.
• M. Q. Martindale, J. Q. Henry, Ctenophora, in S. F. Gilbert, A. M. Raunio, Embryology: Constructing the Organism, Sinauer, 1997, p. 87
• C.E. Mills. Internet 1998-present. Phylum Ctenophora: list of all valid species names. Web page established March 1998, last updated (see date at end of page).
• M. Podar, S. H. D. Haddock, M. L. Sogin, G. R. Harbison, A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes, Molecular Phylogenetics and Evolution, 21, 2001, p. 218
• T. A. Shiganova, Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure, Fisheries Oceanography, 1998, p. 305
• G. D. Stanley, W. Stürmer, The first fossil ctenophore from the lower devonian of West Germany, Nature 303, 1983, p. 518

External links

• University of Washington - Ctenophores
• Ctenophores from the São Sebastião Channel, Brazil