A bioluminescent chaetognath
Haddock, S.H.D. and J.F. Case. (1994). Nature 367: 225-226.

The ability to produce light is especially widespread among marine zooplankton, where the only major phylum without a luminous species has been thought to be the Chaetognatha. These carnivorous arrow worms are found throughout the world's oceans, often second only to copepods in abundance. We recently discovered endogenous bioluminescence in a well- known bathypelagic chaetognath. This is the first addition to the roster of luminescent phyla in more than 50 years.

We first noted chaetognath bioluminescence the Johnson-Sea-Link submersible on cruises with E. A. Widder near the Bahamas Islands. On three dives, at 870, 850, and 760 m, a chaetognath with an orange-pigmented gut darted away, leaving a plume of luminescence.

Chaetognaths were subsequently examined in collections from the North Pacific Ocean on cruises with J. J. Childress. Luminescence was repeatedly evoked in specimens of Caecosagitta macrocephala, a cosmopolitan species generally found at depths greater than 700 m (Fig. 1a). Luminescence was not produced Eukrohnia fowleri, the other common species with an orange gut, nor by nine other chaetognath species examined (identified by E. V. Thuesen).

In marine invertebrates without bacterial symbionts, luminescence is produced through the oxidation of a light-producing compound (luciferin), mediated by a calcium-activated photoprotein, or by an enzyme (luciferase). Methanolic extracts of C. macrocephala contained coelenterazine, the luciferin of cnidarians, ctenophores, radiolarians, and some squid, fish, and crustaceans. Aqueous extracts added to coelen-terazine showed high levels of luciferase activity. (Substrates for the assays were provided by O. Shimomura and S. Inoue). No calcium-activated photoprotein was detected, and an assay for bacterial luciferase performed by M. G. Haygood and G. Mowlds was also negative. These results indicate that light is produced by a coelenterazine-luciferase reaction, making Chaetognatha the seventh phylum known to employ coelenterazine for its luminescence.

Light is produced at the midpoint of the body by large vacuolar cells on the edges of the anterior fins. Ovoid or fusiform membrane-bound inclusions within these cells are autofluorescent to varying degrees, a trait that has been correlated with the location of luminescent sources in many taxa. The fluorescent subcellular bodies are likely sites for storage of the components of the luminescent reaction. Most contain a dense paracrystalline matrix with small spherical inclusions. Others, even within the same cell, lack internal organization, possibly indicating organelles in which the luminescent compounds have reacted.

Although the luminous bodies are visible to the naked eye and may even appear in a published micrograph, they have not been included in previous descriptions of this species These omissions, as well as the failure to note bioluminescence, may be due in part to the poor condition of specimens examined in the past; the insulated closing cod end of the 10-m² Tucker trawl used in this study recovers animals in excellent condition.

Chaetognaths are commonly allied with pseudocoelomates (=Aschelminthes) and with deuterostomes, but recent molecular work supports the view that they diverged near the roots of the Metazoa. Based on this early divergence and on the uniqueness of the light-producing cells, it appears that luminescence evolved independently in Caecosagitta macrocephala, although luciferin could be obtained from dietary sources.

Because luminescence is normally produced in conjunction with an escape response, the cloud of light appears to function as a diversionary display, a commonly hypothesized role for expelled luminescence. This remarkable adaptation highlights the importance of bioluminescence in the interactions among marine organisms and demonstrates the value of in situ observations for understanding life in the sea.