Acquisition and use of nematocysts by cnidarian predators
Introduction
Nematocysts, cnidocysts used to inject venom, offer a formidable defense from predators, but despite this weaponry numerous animals from many phyla prey on cnidarians (Salvini-Plawen, 1972, Ates, 1989, Ates, 1991, Arai, 2005). Some of these predators acquire unfired nematocysts from their prey and store them in functional form within their own cells; the acquired nematocysts are referred to as kleptocnidae. While aeolid nudibranchs are known for sequestering nematocysts from their prey (reviewed in Greenwood, 1988), one ctenophore species, Haeckelia rubra, preys upon narcomedusae and incorporates nematocysts into its own tentacles (Carré and Carré, 1980, Mills and Miller, 1984, Carré et al., 1989). Some turbellarian flatworms also acquire nematocysts from their prey and store them in cells on their dorsal surface (reviewed by Karling, 1966). Because virtually no additional work (since that already cited) has been published on the use of nematocysts by ctenophores or flatworms, this review focuses on the acquisition and use of nematocysts by aeolid nudibranchs. Excellent reviews by Harris (1973) and Todd (1981) detail many aspects of nudibranch ecology including the use of kleptocnidae; this review concentrates on research published since the last review of nudibranch nematocysts (Greenwood, 1988). Because this Toxicon issue focuses on cnidarian toxins and venoms, this review goes into most depth on how nudibranchs protect themselves from the discharging nematocysts of their prey and how the nudibranchs use acquired nematocysts, or kleptocnidae.
Section snippets
Defensive effectiveness of cnidarian nematocysts
Nematocysts are defensive weapons but, as Mariscal (1974) points out, it is difficult to separate experimentally the defensive effects of nematocysts from the defensive effects of other cnidarian chemicals. In an attempt to discern specific effects of nematocysts, Stachowicz and Lindquist (2000) investigated the relative importance of hydroid nematocysts as defense against predators. They found that pinfish did not consume hydroid species with penetrating nematocysts (basitrichous isorhizas and
Physical protection from nematocyst discharge
Many aeolids have a hard cuticle covering the epithelium of the buccal cavity and the esophagus (Edmunds, 1966). The cuticle prevents damage from nematocyst discharge during feeding because nematocysts do not penetrate it. Recent work confirms that this cuticle is chitin (Martin et al., 2007a).
Most cells of the skin and stomach epithelia of aeolid nudibranchs contain intracellular ovoid discs called spindles (Fig. 1) (Henneguy, 1925, Graham, 1938), but the protective function of these spindles
Mucus protection from nematocyst discharge
A mucus layer provides a physical layer of protection (Boutan, 1898, Grosvenor, 1903, Graham, 1938, Salvini-Plawen, 1972, Martin and Walther, 2003), and several authors suggest the possibility of some sort of acclimation to the prey's discharging nematocysts that aids the mucus defense (Grosvenor, 1903, Conklin and Mariscal, 1977). Mauch and Elliott (1997) provided the first direct evidence that the mucus from a cnidarian predator protects it from the prey's nematocyst discharge. Mauch and
Acquisition and storage of kleptocnidae
For those aeolid nudibranchs that store nematocysts in their own cells, unfired nematocysts pass through the digestive diverticula and are engulfed by cnidophage cells within the slugs’ cnidosacs near the tips of the dorsal cerata (Fig. 2). Several factors may contribute to preventing nematocyst discharge during transit through the nudibranch's gut. As mentioned above, nudibranch mucus may inhibit discharge, either chemically (as suggested by Greenwood et al., 2004), or by physically insulating
Kleptocnidae function
While kleptocnidae in aeolid nudibranchs are generally considered defensive, there may be other functions. Two published observations showed nudibranch kleptocnidae were used to attack cnidarian prey during feeding (Bergh, 1862, Tardy, 1964). Several researchers discussed the possibility that kleptocnidae are stored in cnidosacs as a means of sequestering these potentially dangerous products of the nudibranch's prey (Grosvenor, 1903, Graham, 1938, Streble, 1968), and this idea has resurfaced
The future
Several fundamental questions of nematocyst toxinology include: (1) how is nematocyst discharge controlled; (2) how can nematocyst discharge be inhibited; and (3) what are some effective defenses from discharging nematocysts? Research over the last two decades (and before) has shown that aeolid nudibranchs and their cnidarian prey can serve as useful model systems to investigate each of these questions. Continued work on how these predators steal and use nematocysts should continue to
Acknowledgements
Research in our laboratory is supported by NIH grant number P20 RR-016463 from the INBRE Program of the National Center for Research Resources, the National Science Foundation (USE-8852191), the National Institutes of Health (1R15 GM44130-01A2), the Howard Hughes Medical Institute, and Colby College. The ceras tip illustration was kindly provided by TRG.
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