Gulf of Mexico Origin, Waters, and Biota: Volume I, Biodiversity

64. Kinorhyncha of the Gulf of Mexico

Kinorhynchs are microscopic, marine, free-living, segmented invertebrates with a head that bears a retractable, oral cone ringed by spines; most species are less than 1 mm in length (Kristensen and Higgins 1991). The 13 chitinous segments are distinctive; the terminal segment often has pronounced lateral end spines. Movement of living kinorhynchs is also distinctive, generated by the rhythmical inversion of the first zonite (head), with its spinous scalids serving as anchors to allow the body to be dragged forward . Their range extends from intertidal beaches to at least several thousand meters depth, and from the polar seas to the tropics. Most occur on or in marine sands or muds, but some occur on algal mats, in algal holdfasts, or less commonly, on sessile macrofauna such as sponges, hydroids, and ectoprocts (Higgins 1977, 1978, 1983). Kinorhynchs are dioecious, and sexual dimorphism is obvious in several genera, including Echinoderes, Pycnophyes , and Kinorhynchus (see Kristensen and Higgins 1991). Males sometimes can be distinguished by the presence of paired penile spines. Fertilization is assumed to be internal, but mating has not been reported. Fertilized ova develop within egg cases deposited in the environment; direct development results in juveniles emerging from the egg case, and they increase in size by molting until they attain the 13 segments characteristic of adult members of the phylum. Because they molt, Kinorhyncha are ecdysozoans and share many morphological traits with the phyla Priapulida and Loricifera, and they commonly are included within the group Scalidophora. A few systematists ally the phyla Priapulida, Kinorhyncha, Loricifera, and Nematomorpha within the phylum Cephalorhyncha (Malakhov 1980, Adrianov, Malakhov, and Yushin 1990). Kinorhynchs typically are summarily treated in most invertebrate texts, such that most invertebrate biologists are not familiar with the taxon. This is unfortunate, as species identification is often relatively simple and primarily based on the morphology and numbers and position of scalids, spines, and sensory spots on the different body segments or zonites. Also, because their exoskeleton is hydrophobic, causing them to adhere to the air-water interface in samples, kinorhynchs are among the easiest meiofauna to collect. Bubbling air though a sample usually concentrates kinorhynchs on the water surface, where they can be skimmed off (Higgins 1988). Kinorhynchs usually are reported in low densities (<15 specimens/10 cm2 ); however, in some habitats kinorhynchs are abun1129 64 Kinorhyncha of the Gulf of Mexico Thomas C. Shirley  Kinorhyncha. After Higgins 1983. 1130 ~ Kinorhyncha of the thick, cuticular wall of the segments for spines. Obviously, a new description is warranted for E. steineri. Echinoderes cf. coulli has been collected infrequently from salt marsh sites and nearshore areas along the Louisiana coast, although the species has not been reported in publications (J. Fleeger, Louisiana State University, personal communication); this may be an undescribed species that resembles Echinoderes coulli (R. P. Higgins, personal communication). Murrell and Fleeger (1989) reported that kinorhynchs were the third most abundant meiofaunal taxon in Timbalier Bay, Louisiana, and the shelf area immediately offshore. They found a number of species of kinorhynchs, but only recorded Echinoderes sp. However, kinorhynchs occur throughout the Gulf of Mexico in high-salinity estuaries, bays, sandy beaches, from the shallow subtidal to at least 550 m depth (Church et al. 2007). In general, most collections come from intertidal or depths less than 100 m and extend from Veracruz , Mexico, and Brownsville, Texas, to Goodland Bay (Marco, Florida). Offshore records, from depths of more than 100 m, include stations from the continental shelf south of Louisiana (maximum recorded depth 845 m), and extending off the shelf to 1251 m; south of Alabama (maximum recorded depth 2470 m; south of Pensacola, Florida, to a maximum record depth of 2800 m (unpublished information, R. P. Higgins); these depths represent only those kinorhynchs collected within the Gulf of Mexico . Kinorhynchs have been reported from numerous faunal surveys, but most specimens have been identified only to phyletic rank. Five genera of kinorhynchs (Echinoderes, Pycnophyes, Semnoderes, Trachydemus, and Centroderes) were reported from the outer continental shelf of the western Gulf of Mexico, contributing up to 7.3% of the meiofauna , but no species were listed (Alexander et al. 1981, Danek et al. 1985). Representatives from these surveys and others in the Gulf of Mexico are present in the collections of the U.S. National Museum of Natural History, but have not been verified or identified to species. This small phylum of enigmatic organisms pleads for additional research in the Gulf of Mexico. Abbreviations The following abbreviations are used in the accompanying checklist under “Habitat-Biology”: ben = benthic; end = endemic to the Gulf of Mexico; est = estuarine; ins = inshore; sft = soft substrates (mud, sands, clays). Abbreviations used under the heading “Overall Geographic Range” are as follows: GO = known only from the Gulf of Mexico; dant, exceeding 250 specimens/10 cm2 (Pfannkuche and Thiel 1987, Giere 1993). Kinorhynchs have been reported at densities exceeding 250 specimens/10 cm2 on the continental shelf off the Louisiana coast, sometimes exceeding 10% of the total meiofauna abundance (Radziejewska et al. 1996). The role of kinorhynchs in food webs and energy flow remains poorly known. However, there are 4 reports of kinorhynchs found in a digestive tract. Milward (1982) recorded kinorhynchs in the stomachs of “mudskippers,” fish of the family Gobiidae, Periophthalmus spp. and Scartelaos histophorus (Valenciennes 1837), mainly taken from mangrove mudflats near Townsville, Australia; Pekkarinen (1985) reported kinorhynchs in the gill pouches of Macoma balthica (Linnaeus, 1758) in the Baltic Sea near Tvarminne, Finland; Echinoderes sp. was found in the stomach of the bivalve mollusc, Aulacoma ater Molina, 1782 (see Osório and Iguain 1987); and in a recent paper by Martorelli and Higgins (2004), the kinorhynchs Pycnophyes anomalus Matorelli and Higgins, 2004, P. neuhausi Matorelli and Higgins, 2004, and Condyloderes storchi Matorelli and Higgins, 2004, were found in the stomachs of the Argentine red shrimp, Pleoticus muelleri (Bate, 1888) from the Argentine coast of Patagonia. Worldwide, approximately 150 species of kinorhynchs have been described; however, many remain to be described. Echinoderes is by far the largest genus, with 63 valid species (Sorensen, Heiner, and Ziemer 2005). Perhaps the most comprehensive taxonomic key to the phylum is by Higgins (1983). Kinorhynchs were not included in the original Bulletin 89, and only a single species from the Gulf of Mexico has been reported (Chitwood 1951), although specimens from as many as 5 genera have been reported (Alexander et al. 1981, Danek et al. 1985). Echinoderes steineri was described from Mud Island, Aransas Bay, in 1.3 m of water and remains the only kinorhynch species described from the Gulf of Mexico (Chitwood 1951); no other specimens of the species have been collected. The original description consisted of a single page with one accompanying figure of an adult female. Chitwood (1951) included E. steineri within the genus Echinoderella, a genus later recognized to represent Echinoderes without pigmented eyespots. Eyespots are seen only in living animals, and Echinoderella was synonomized with Echinoderes by Karling (1954). To complicate matters, Chitwood (1951) misspelled Echinoderella as Echinodella in his figure. Higgins (1983) pointed out that lateral spines were probably lacking on segments 3, 5, and 6 in E. steineri, and that Chitwood (1951) may have mistaken the optical section view Shirley ~ 1131 9. Higgins, R. P. 1983. The Atlantic barrier reef ecosystem at Carrie Bow Cay, Belize. II. Kinorhyncha. Smithsonian Contributions to the Marine Sciences 18: 1–131. 10. Higgins, R. P. 1988. Kinorhyncha. Pp. 328–331 in R. P. Higgins and H. Thiel, eds. Introduction to the Study of Meiofauna . Smithsonian Institution Press. Washington, D.C. 11. Karling, T. G. 1954. Echinoderes levanderin. sp. (Kinorhyncha ) aus der Ostee. Arkiv Fur Zoologi, Series 2, 7(10): 189–192. 12. Kristensen, R. M., and R. P. Higgins. 1991. Pp. 377–404 in F. W. Harrison, ed. Microscopic Anatomy of Invertebrates. Volume 4: Aschelminthes. Wiley-Liss, New York. 13. Malakhov, V. V. 1980. Cephalorhyncha, a new type of animal phylum of animal kingdom uniting Priapulida, Kinorhyncha, Gordiacea, and a system of Aschelminthes worms. Zoologicheskii Zhurnal 59(4): 485–499. [In Russian, English summary.] 14. Martorelli, S., and R. P. Higgins. 2004. Kinorhyncha from the stomach of the shrimp Pleoticus muelleri (Bate, 1888) from Comodoro Rivadavia, Argentina. Zoologischer Anzeiger 243: 85–98. 15. Milward, N. E. 1982. Mangrove-dependent biota. Pp. 121–139 in B. F. Clough, ed. Mangrove Ecosystems in Australia. Structure, Function and Management. Australian Institute of Marine Science, Townsville. 16. Murrell, M. C., and J. W. Fleeger. 1989. Meiofauna abundance on the Gulf of Mexico continental shelf affected by hypoxia. Continental Shelf Research 9: 1049–1062. 17. Osório, C., and R. Iguain. 1987. Kinorhyncha en Chile: Presencia de Echinoderes Dujardin [sic], 1851. Boletín de la Sociedad de Biología de Concepción 58: 119–120. 18. Pekkarinen, M. 1985. Exoskeletons of kinorhynchs in tissues of the bivalve Macoma balthica in the Baltic Sea, southwestern Finland. Annales Zoologici Fennici 22: 407–410. 19. Pfannkuche, O., and H. Thiel. 1987. Meiobenthic stocks and benthic activity on the NE Svalbard shelf and in the Nansen Basin. Polar Biology 7: 253–266. 20. Radziejewska, T., J. W. Fleeger, N. N. Rabalais, and K. R. Carman . 1996. Meiofauna and sediment chloroplastic pigments on the continental shelf offLouisiana, U.S.A. Continental Shelf Research 16(13): 1699–1723. 21. Sorensen, M. V., I. Heiner, and O. Ziemer. 2005. A new species of Echinoderes from Florida (Kinorhyncha: Cyclorhagida ). Proceedings of the Biological Society of Washington 118(3): 499–508. GMx = Gulf of Mexico; SE = southeastern United States. Abbreviations used under the heading “GMx range” are as follows: ne = northeast; nw = northwest. Acknowledgments I thank Drs. R. Higgins (National Museum of Natural History , retired) and J. Fleeger (Louisiana State University) for their assistance. References 1. Adrianov, A. V., V. V. Malakhov, and Y. Y. Yushin. 1990. Loricifera—a new taxon of marine invertebrates. Soviet Journal of Marine Biology 15: 136–138. 2. Alexander, S. K., P. N. Boothe, R. W. Flint, C. S. Giam, J. S. Holland, G. Neff, W. E. Pequegnat, P. Powell, N. N. Rabalais , J. R. Schwarz, P. J. Szanniszlo, C. Venn, D. E. Wohlschlag, and R. Yoshiyama. 1981. Benthic biota. Pp. 83–136 in R. W. Flint and N. N. Rabalais, eds. Environmental Studies of a Marine Ecosystem. University of Texas Press, Austin. 3. Chitwood,B. G.1951.Echinoderellasteinerinewspecies(Scolecida ,Echinodera).TexasJournalofScience3(1):113–114. 4. Church, R. D., D. J. Warren, R. Cullimore, L. Johnston, W. Schroeder, W. Patterson, T. Shirley, M. Kilgour, N. Morris, and J. Moore. 2007. Archaeological and Biological Analysis of World War II Shipwrecks in the Gulf of Mexico: Artificial Reef Effect in Deep Water. U.S. Dept. of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans, Louisiana. OCS Study MMS 2007-015. 387 pp. 5. Danek, L. J., M. S. Tomlinson, G. H. Tourtellotte, W. A. Tucker, K. M. Erickson, G. K. Foster, G. S. Lewbel, G. S. Boland, and J. S. Baker. 1985. Southwest Florida Shelf Benthic Communities Study. Year 4 Annual Report, Volume 1, Report 85-0073 for the U.S. Department of the Interior Minerals Management Service, Gulf of Mexico Outer Continental Shelf Region. 6. Giere, O. 1993. Meiobenthology. The Microscopic Fauna in Aquatic Sediments. Springer-Verlag, Heidelberg. 328 pp. 7. Higgins, R. P. 1977. Two new species of Echinoderes (Kinorhyncha) from South Carolina. Transactions of the American Microscopical Society 97(2): 340–354. 8. Higgins, R. P. 1978. Echinoderes gerardin. sp. and E. riedli (Kinorhyncha) from the Gulf of Tunis. Transactions of the American Microscopical Society 97(2): 171–180. Submitted: August 2007 Accepted: September 2007 1132 ~ Kinorhyncha Checklist of kinorhynchs (Kinorhyncha) from the Gulf of Mexico. Taxon HabitatBiology Depth (m) Overall geographic range GMx range References/ Endnotes Phylum: Kinorhyncha Order: Cyclorhagia Family: Echinoderidae Echinoderes steineri (Chitwood, 1951) ben, end, est, sft 1.3 GO nw 3, 9 Echinoderes cf. coulli Higgins, 1977 ben, est, sft, ins 0–10 SE, GMx nw, ne 9, 16 ...