Structural diversity, systematics, and evolution of cnidae
Introduction
Nematocysts are the sine qua non of phylum Cnidaria—all cnidarians and only cnidarians produce them. At least some types of nematocysts are associated with venom; this is the source of the sting of jellyfish, for example. Nematocysts are the means by which cnidarians protect themselves and capture prey—cnidarians are exclusively carnivorous (e.g. Hand and Fautin, 1988) although some that live in shallow water harbor photoendosymbionts from which they may derive fixed carbon (e.g. Muscatine, 1961, Muscatine and Cernichiari, 1969). Each microscopic capsule (length range is about 20–200 μm) is secreted by the Golgi apparatus of a cell specialized for this function, termed a nematoblast (Watson and Wood, 1988). Thus, despite common usage to the contrary, a nematocyst is not a “stinging cell”—it is the capsule made by the cell that delivers the sting.
Nematocysts constitute one of three categories of such intracellular secretory products of cnidarians. The others are ptychocysts and spirocysts, capsules that occur in only a limited diversity of cnidarians (see Section 3 below). Bozhenova (1988: 71) expressed a distinctly minority, and somewhat outdated, view in declaring, “The division of cnidae into spirocysts, nematocysts and ptychocysts seems to be groundless.” The collective term for these capsules is cnida (plural cnidae), derived from the Greek for nettle (κνιδη) (knide). An alternative term for nematocyst is cnidocyst (Weill, 1934a). The cells that make the capsules are cnidoblasts (specific types are nematoblasts, ptychoblasts, and spiroblasts), with the corresponding mature cells cnidocytes (and nematocytes, ptychocytes, and spirocytes) (Watson and Wood, 1988). The word Cnidaria is currently the preferred term for the phylum that some still call Coelenterata, but, as van der Land (2003) has argued, there is no good scientific reason to replace Coelenterata with Cnidaria, so the two are interchangeable in modern usage.
Cnidae are, according to Mariscal (1974: 130), “among the largest and most complex intracellular secretion products known.” Upon receipt of an appropriate chemical and/or mechanical stimulus (reviewed by Anderson and Bouchard, 2009), a nematocyst discharges so the tubule that had been coiled and twisted inside the capsule everts, to be emitted from one end of the capsule, which opens as part of the discharge process. This discharge is among the fastest cellular processes (Holstein and Tardent, 1984). It is the discharged nematocyst that gave rise to the name of the structure, literally “thread capsule” (for eversion to occur, clearly the tubule must be hollow, which is why the term thread or filament is unsuitable for it: Watson and Wood, 1988). A spirocyst capsule had been considered single-walled (e.g. Hyman, 1940, Westfall, 1965), but it is actually double-walled like that of a nematocyst, although thinner (Mariscal and McLean, 1976). The nature of the ptychocyst capsule wall was not specified in the publication describing that cnida type (Mariscal et al., 1977). A spirocyst tubule, like that of a nematocyst, is “helically folded with multiple pleats in length, but only three in circumference”; a ptychocyst tubule differs in being “folded accordion-like in circumference into a series of stacked pleats” (Mariscal et al., 1977: 396).
By contrast with the complexity of these secretory products, cnidarians are structurally simple, at the tissue grade of organization, composed of two epithelia, the ectoderm and endoderm. The ectoderm is also referred to as the epidermis and the endoderm as the gastrodermis. Hyman (1940) advocated using epidermis and gastrodermis, reserving the other terms for embryological layers, but she later (Hyman, 1967) repudiated that position, recognizing that the terms ectoderm and endoderm had been coined for adult coelenterates and were applied, in the context of recapitulation, to embryonic layers of “higher” animals (as discussed by Fautin and Mariscal, 1991). Between the epithelia lies the mesoglea, which varies from entirely acellular (as in hydrozoans: e.g. Thomas and Edwards, 1991) to rather rich in cells (e.g. Hyman, 1940). Three-dimensionality is achieved by folding these sheets of cells, which prompted Shick (1991: 3) to quip that “Sea anemones … are at the ‘origami’ level of construction.” In situ, a cnida is oriented with the end that opens upon discharge near the free surface of the cell layer, so the tubule is shot into the gastrovascular space (for a cnida in a mesenterial filament, for example) or outside the animal (for a cnida in a tentacle, for example).
Cnidocytes are part of one or both of these epithelia, depending on the taxon. In most cnidarians, most nematocytes are ectodermal, occurring largely in the tentacles: for example, more than 95% of nematocytes of Hydra attenuata are in the tentacles, where their number increases from base to tip (Bode and Flick, 1976). In non-skeletalized organisms, such as medusae and sea anemones, nematocysts typically occur elsewhere on the outer surface of the animal. Scyphomedusae have endodermal nematocytes in the gastric cirri (Arai, 1997). Members of Anthozoa also have nematocytes in the endoderm; the mesenteries are edged by filaments containing both gland cells that produce digestive enzymes (summarized by Shick, 1991) and nematocysts that may function in subduing, if not digesting, prey. Spirocysts are typically more abundant than nematocysts in tentacles of sea anemones and their relatives; the amazing number of 43 million “Nesselkapseln” in one tentacle of the common European sea anemone Anemonia sulcata reported by Möbius (1866) (who called the animal Anthea cereus) is likely to have been mostly spirocysts—which Bedot distinguished as a separate category only in 1890.
Mackie (2002: 1650) called nematocysts “the cnidarians’ secret weapon.” He continued, “They have enabled the group to achieve enormous success as predators with little of the investment in elaborate sensory and morphological specialization that characterizes most predators. Thus, cnidarians have prevailed despite their exceedingly simple basic body plan.” I am unaware of figures for the cost of producing nematocysts, individually or on a per animal basis, but their continual production must be a significant portion of an animal's energy budget: they are complex; an individual possesses large numbers of them [about 30% of the roughly 11,000 cells in a polyp of Hydra magnipapillata are nematocytes and nematoblasts (Sugiyama and Fujisawa, 1977), and a large colony of the siphonophore Nanomia cara is estimated to have six million nematocysts (Mackie, 1999)]; and each is used but once, with many typically discharging during an offensive or defensive act [Bode and Flick (1976: 31) calculated that nearly 25% of nematocytes—or about 7500 cells—are lost from the tentacles of H. attenuata each day].
Because cnidae are so central to both the biology and the concept of cnidarians, papers on them are part of the proceedings of all seven international conferences on coelenterate biology to have been held (Rees, 1966, Tokioka, 1973, Mackie, 1976, Tardent and Tardent, 1980, Williams et al., 1991, den Hartog et al., 1997, Fautin et al., 2004). Other volumes concerned with cnidarians that contain important information on cnidae include The Biology of Hydra and of Some Other Coelenterates 1961 (Lenhoff and Loomis, 1961), Coelenterate Biology: Reviews and New Perspectives (Muscatine and Lenhoff, 1974), Hydra: Research Methods (Lenhoff, 1983), Microscopic Anatomy of Invertebrates, volume 2: Placozoa, Porifera, Cnidaria, and Ctenophora (Harrison and Westfall, 1991), a dedicated issue of volume 80 of the Canadian Journal of Zoology, and some of the proceedings of hydrozoan workshops such as Bouillon et al. (1987) and Mills et al. (2000). Review articles on cnidae in general or only nematocysts include Hand, 1961, Halstead, 1965 (who focused on medical aspects of stinging), Picken and Skaer, 1966, Mariscal, 1974, Mariscal, 1984, and Östman (2000). The Biology of Nematocysts (Hessinger and Lenhoff, 1988) comprises the proceedings of an international symposium devoted to these intriguing structures. Some of these sources discuss hypotheses of how nematocysts discharge, which is still unresolved; nematocysts were once considered independent effectors, but it is now clear that the animal can exert control over their discharge (see, e.g., Fautin and Mariscal, 1991, Shick, 1991, Kass-Simon and Scappaticci, 2002; Anderson and Bouchard, 2009) although isolated capsules of most types are capable of discharge (Greenwood et al., 2003).
Section snippets
Diversity of cnidae
The most widely-used classification, which recognizes about 30 morphological types of nematocysts, is derived from the work of Weill, 1930, Weill, 1934a, Weill, 1934b) who, in two large volumes, inventoried nematocysts (and spirocysts) from many species, and raised issues of biology and making distinctions that still trouble biologists (Fautin, 1988). Weill's classification of nematocysts, which “has been tinkered with and debated almost since it was proposed” (Fautin, 1988: 489), relies
Taxonomic and systematic value of nematocysts
At the highest taxonomic level, the systematic implication of nematocysts is clear. All cnidarians, and only cnidarians, produce them. Few other phyla are diagnosable by a single unambiguous feature such as this (members of Cnidaria share other features that reinforce the monophyly of the group—but none is as diagnostic as nematocysts).
What animals are most closely related evolutionarily to cnidarians is uncertain, but one candidate is ctenophores. Aside from the fact that many are gelatinous
Evolution and cnidae
The distinctiveness of cnidae, the production of which unambiguously diagnoses a cnidarian, also make them unsuitable for determining evolutionary relationships of the phylum—no organism that otherwise seems closely related to cnidarians creates similar structures. The uniqueness of cnidae has led to theories about their restriction to these animals because of symbiosis. Evidence that Shostak (1993) summarized for the “symbiogenetic theory for the origins of Cnidaria” is based on studies in
Acknowledgments
Support was contributed by US National Science Foundation grants DEB99-78106 in the program Partnerships for Enhancing Expertise in Taxonomy (PEET), and EF05-31779 in the program Assembling the Tree of Life. I thank many cnidarian biologists, Bill Kem, and Jonathan Deeds for being so responsive to my requests for information, and Carla Marrs, Sarah Mahoney, and Katie Soldan for help in preparing the manuscript.
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