Scientia Marina, Vol 74, No 2 (2010)

Feeding on protists and particulates by the leptocephali of the worm eels Myrophis spp. (Teleostei: Anguilliformes: Ophichthidae), and the potential energy contribution of large aloricate protozoa


https://doi.org/10.3989/scimar.2010.74n2339

John Jeffrey Govoni
NOAA, National Ocean Service, National Centers for Coastal Ocean Science, Center for Coastal Fisheries and Habitat Research , United States

Abstract


The food sources of the leptocephali of the teleostean superorder Elopomorpha have been controversial, yet observations on the leptocephali of the worm eels, Myrophis spp. (family Ophichthidae) collected in the northern Gulf of Mexico indicate active, not passive, feeding. Leptocephali had protists in their alimentary canals. Estimates of the physiological energetics of worm eels indicate that large aloricate protozoa including ciliates could provide substantial energy to these leptocephali toward the end of the premetamorphic and metamorphic stages, given the low energy requirements of metamorphosing leptocephali. Global ocean warming will likely force a shift in oceanic food webs; a shift away from large protozoa toward smaller protists is possible. Such a disruption of the oceanic food webs could further compromise the survival of leptocephali.

Keywords


Myrophis; leptocephali; feeding; protozoa; ciliates

Full Text:


PDF

References


Alikunhi, K.H. and S.N. Rao. – 1951. Notes on the metamorphosis of Elops saurus Linn. and Megalops cyprinoides (Broussonet) with observations on their growth. J. Zoo. Soc. India, 3: 99-109.

Bishop, R.E. and J.J. Torres. – 1999. Leptocephalus energetics: metabolism and excretion. J. Exp. Biol., 202: 2485-2439. PMid:10460735

Bishop, R.E., J.J. Torres and R.E. Crabtree. – 2000. Chemical composition and growth indices in leptocephalus larvae. Mar. Biol., 137: 205-214. doi:10.1007/s002270000362

Bonhommeau, S., E. Chassot and E. Rivot. – 2008. Fluctuations in European eel (Anguilla Anguilla) recruitment resulting from environmental changes in the Sargasso Sea. Fish. Oceanogr., 17: 32-44.

Crawford, D.W. – 1993. Some observations on morphological variation in the red-water ciliate Mesodinium rubrum. J. Mar. Biol. Assoc., U. K., 73: 975-978. doi:10.1017/S002531540003486X

Crawford, S. and D.K. Stoecker. – 1996. Carbon content, dark respiration and mortality of the mixotrophic planktonic ciliate Strombidium capitatum. Mar. Biol., 126: 415-422. doi:10.1007/BF00354623

Desaunay, Y. and D. Guerault. – 1997. Seasonal and long-term changes in biometrics of eel larvae: a possible relationship between recruitment variation and North Atlantic ecosystem productivity. J. Fish Biol. (Suppl. A), 51: 317-339. doi:10.1111/j.1095-8649.1997.tb06106.x

Døving, K.B. and A.O. Kasumyan. – 2008. Chemoreception. In: R.N Fynn and B.G. Kapoor (eds.), Fish Larval Physiology Sensory Physiology, Part 4, Chapter 11, pp. 331-352. Academic Press, New York.

Figueiredo, G.M., R.D.M. Nash and D.J.S. Montagnes. – 2005. The role of the generally unrecognized microprey source as food for larval fish in the Irish Sea. Mar. Biol., 148: 395-404. doi:10.1007/s00227-005-0088-0

Figueiredo, G.M., R.D.M. Nash and D.J.S. Montagnes. – 2007. Do protozoa contribute significantly to the diet of larval fish in the Irish Sea? J. Mar. Biol. Assoc., U. K., 87: 843-850. doi:10.1017/S002531540705713X

Finlay, B.J. and U. Uhlig. – 1981. Calorific and carbon values of marine and freshwater protozoa. Helgol. Wiss. Meeresunters., 34: 401-412. doi:10.1007/BF01995913

Friedland, K.D., M. Miller and B. Knights. – 2006. Oceanic changes in the Sasrgasso Sea and declines in recruitment of the European eel. ICES J. Mar. Sci., 64: 519-530. doi:10.1093/icesjms/fsm022

Fukami, K., A. Watanabe, S. Fujita, K. Yamaoka and T. Nishijima. – 1999. Predation on naked protozoan microzooplankton by fish larvae. Mar. Ecol. Prog. Ser., 185: 285-291. doi:10.3354/meps185285

Govoni, J.J. – 2005. Fisheries Oceanography and the ecology of the early life histories of fishes: a perspective over fifty years. Sci. Mar., 69 (Suppl. 1): 125-137.

Govoni, J.J. and A.J. Chester. – 1990. Diet composition of larval Leiostomus xanthurus in and about the Mississippi River Plume. J. Plankton Res., 12: 819-830. doi:10.1093/plankt/12.4.819

Govoni, J.J., D.E. Hoss and A.J. Chester. – 1983. Comparative feeding of three species of larval fishes in the northern Gulf of Mexico: Brevoortia patronus, Leiostomus xanthurus, and Micropogonias undulates. Mar. Ecol. Prog. Ser., 13: 189-199. doi:10.3354/meps013189

Govoni, J.J., A.J. Chester, D.E. Hoss and P.B. Ortner. – 1985. An observation of episodic feeding and growth of larval Leiostomus xanthurus in the northern Gulf of Mexico. J. Plankton Res., 7: 137-146. doi:10.1093/plankt/7.1.137

Govoni, J.J., P.B. Ortner, F. Al-Yamani and L.C. Hill. – 1986. Selective feeding of spot, Leiostomus xanthurus, larvae in the northern Gulf of Mexico. Mar. Ecol. Prog. Ser., 28: 175-183. doi:10.3354/meps028175

Harnden, C.W., R.E. Crabtree and J.M. Shenker. – 1999. Onshore transport of elopomorph leptocephali and glass eels (Pisces: Osteichthyes) in the Florida Keys. Gulf Mexico Sci., 17: 17-26.

Hulet, W.H. – 1978. Structure and functional development of the eel leptocephalus Ariosoma balearicum (DeLa Roche, 1809). Phil. Trans. Roy. Soc. London, Biol. Sci., 252: 107-138.

Hulet, W.H. and C.R. Robins. – 1989. The evolutionary significance of the leptocephalus larva. In: E.B. Böhlke (ed.), Fishes of the Western North Atlantic, Leptocephali Part 9, Vol. 2, pp. 669-677. New Haven, Connecticut: Sears Foundation for Marine Research, Yale University.

Hureau, J.C. and Th. Monod. – 1973. Check-list of the fishes of the north-eastern Atlantic and the Mediterranean. Vol. 1. Presses Universitaires de France, Vendôme.

Hunt von Herbing, I. and S.M. Gallager. – 2000. Foraging behavior in Atlantic cod larvae (Gadus morhua) feeding on a protozoan (Balanion sp.) and a copepod nauplius (Pseudodiaptomus sp.) Mar. Biol., 136: 591-602. doi:10.1007/s002270050719

Leakey, R.J.G., P.H. Burkill and M.A. Sleigh. – 1994. A comparison of fixatives for the estimation of abundance and biovolume of marine planktonic ciliate populations. J. Plankton Res., 136: 375-389. doi:10.1093/plankt/16.4.375

Leiby, M.M. – 1989. Family Ophichthidae: Leptocephali. In: E.B. Böhlke (ed.), Fishes of the Western North Atlantic, Leptocephali, Part 9, Vol. 2, pp. 764-897. New Haven: Sears Foundation for Marine Research, Yale University.

Lessard, E.J. and M.C. Murrell. – 1996. Distribution, abundance and size composition of heterotrophic dinoflagellates and ciliates in the Sargasso Sea near Bermuda. Deep-Sea Res., 43: 1045-1065. doi:10.1016/0967-0637(96)00052-0

Liao, I.C. and S.L. Chang. – 2001. Induced spawning and larval rearing of Japanese eel, Anguilla japonica in Taiwan. J. Taiwan Fish. Res., 9: 97-108.

Lindholm, T. and A.-C. Mörk. – 1990. Depth maxima of Mesodinium rubrum (Lohmann) Hamburger and Buddenbrock – examples from a stratified Baltic Sea inlet. Sarsia, 75: 53-64.

Lynn, D.H. and D.J.S. Montagnes. – 1988a. Taxonomic descriptions of some conspicuous species of the family strombidiidae (Ciliophora: oligotrichida) from the Isles of Shoals, Gulf of Maine. J. Mar. Biol. Assoc., U. K., 68: 259-276. doi:10.1017/S0025315400052176

Lynn, D.H. and D.J.S. Montagnes. – 1988b. Taxonomic Descriptions of some conspicuous species of strombilidiine ciliates (Ciliophora: choreostichida) from the Isles of Shoals, Gulf of Maine. J. Mar. Biol. Assoc., U. K., 68: 639-658. doi:10.1017/S0025315400028770

Lynn, D.H., D.J.S. Montagnes, T. Dale, G.L. Gilron and S.L. Strom. – 1991. A reassessment of the genus Strombidinopsis (Ciliophora, Choreotrichida) with descriptions of four new planktonic species and remarks on its taxonomy and phylogeny. J. Mar. Biol. Assoc., U. K., 71: 597-612. doi:10.1017/S0025315400053170

McCosker, J.E. – 1997. The osteology, classification, and relationships of the eel family Ophichthidae. Proc. Calif. Acad. Sci., 41: 1-23.

Miller, M.J. and K. Tsukamoto. – 2004. Introduction to leptocephali biology and identification. Ocean Research Institute, University of Tokyo. Tokyo.

Miller, M.J., S. Kimura, K.D. Friedland, B. Knights, H. Kim, D.J. Jeffyman and K. Tsukamoto. – 2009. Review of ocean-atmospheric factors in the Atlantic and Pacific oceans influencing spawning and recruitment of anguillid eels. In: A. Haro, T. Avery, K. Beal, J. Cooper, R. Cunjak, M. Dadswell, R. Klauda, C. Moffitt, R. Rulifson and K. Smith (eds.), Challenges for diadromous fishes in a dynamic global environment. Bethesda: American Fisheries Society. Symposium 69: 231-249.

Mochioka, N. and M. Iwamizu. – 1996. Diet of anguilloid larvae: leptocephali feed selectively on larvacean houses and fecal pellets. Mar. Biol., 125: 447-452.

Mochioka, N., M. Iwamizu and T. Kanda. – 1993. Leptocephalus eel larvae will feed in aquaria. Environ. Biol. Fish., 36: 381-384. doi:10.1007/BF00012416

Moser, H.G. – 1981. Morphological and functional aspects of marine fish larvae. In: R. Lasker (ed.), Marine fish larvae: morphology, ecology, and relation to fisheries, pp. 90-131. Seattle: Washington: Washington Sea Grant Program, University of Washington Press.

Ohman, M.D., G.H. Theilacker and S.E. Kaupp. – 1991. Immunochemical detection of predation on ciliate protists by larvae of the northern anchovy (Engraulis mordax) Biol. Bull., 181: 500-504. doi:10.2307/1542370

Okamura, A., P. Hideo, Y. Yamada, T. Utoh, N. Mikawa, H. Noriyuki and S. Tanaka. – 2002. Development of lateral line organs in leptocephali of the freshwater eel Anguilla japonica (Teleostei, Anguilliformes). J. Morphol., 254: 81-91. doi:10.1002/jmor.10021 PMid:12219345

Otake, T. – 1996. Fine structure and function of the alimentary canal in leptocephali of the Japanese eel Anguilla japonica. Fish. Sci., 62: 28-34.

Otake, T., K. Nogami and K. Maruyaka. – 1990. Possible food sources of eel leptocephali. La Mer, 28: 218-224.

Otake, T., K. Nogami and K. Maruyaka. – 1993. Dissolved and particulate organic matter as possible food sources for eel leptocephali. Mar. Ecol. Prog. Ser., 92: 27-34. doi:10.3354/meps092027

Pedersen, B.H., B. Uberscha and T. Kurokawa. – 2003. Digestive response and rates of growth in pre-leptocephalus larvae of the Japanese eel Anguilla japonica reared on artificial diets. Aquaculture, 215: 321-338. doi:10.1016/S0044-8486(02)00065-0

Pepin, P. and J.E. Dower. – 2007. Variability in the trophic position of larval fish in a coastal pelagic ecosystem based on stable isotope analysis. J. Plankton Res., 727-737. doi:10.1093/plankt/fbm052

Pfeiler, E. – 1986. Toward an explanation of the developmental strategy in leptocephalus larvae of marine fish. Environ. Biol. Fish., 15: 3-13. doi:10.1007/BF00005385

Pfeiler, E. – 1989. Sensory systems and behavior of premetamorphic and metamorphic leptocephalus larvae. Brain Behav. Evol., 34: 25-34. doi:10.1159/000116488

Pfeiler, E. – 1996. Energetics of metamorphosis in bonefish (Albula sp.) leptocephali: role of keratin sulfate glycosaminoglycan. Fish Physiol. Biochem., 15: 359-362. doi:10.1007/BF02112363

Pfeiler, E. – 1999. Developmental physiology of elopomorph leptocephali. Comparative Biochemistry and Physiology . A – Mol. Integr. Physiol., 123: 113-128. doi:10.1016/S1095-6433(99)00028-8

Pfeiler, E. and J.J. Govoni. – 1993. Metabolic rates in early life history stages of elopomorph fishes. Biol. Bull., 185: 277-283. doi:10.2307/1542007

Pierce, R.W. and J.T. Turner. – 1992. Ecology of planktonic ciliates in marine food webs. Rev. Aquat. Sci., 6: 139-181.

Smith, D.G. – 1984. Elopiformes, Notocanthiformes, and Anguilliformes: Relationships. In: H.G. Moser and W.J. Richards (eds.), Ontogeny and systematics of fishes, pp. 94-102. Lawrence: American Society of Ichthyologist and Herpetologists Special Publication 1.

Smith, D.G. – 1989. Introduction to leptocephali. In: E.B. Böhlke (ed.), Fishes of the Western North Atlantic, Leptocephali Part 9, Volume 2 pp. 657-668. New Haven, Connecticut: Sears Foundation for Marine Research, Yale University.

Stoecker, D.K. and J.J. Govoni. – 1984. Food selection by young larval gulf menhaden (Brevoortia patronus). Mar. Biol., 80: 299-306. doi:10.1007/BF00392825

Stoecker, D.K., A. Taniguchi and A.E. Michaels. – 1989. Abundance of autotrophic, mixotrophic and heterotrophic planktonic ciliates in shelf and slope waters. Mar. Ecol. Prog. Ser., 50: 241-254. doi:10.3354/meps050241

Stoecker, D.K., D.J. Gifford, D.J. and M. Putt. – 1994. Preservation of marine planktonic ciliates: losses and cell shrinkage during fixation. Mar. Ecol. Prog. Ser., 110: 293-299. doi:10.3354/meps110293

Tanaka, H. – 2003. Techniques for larval rearing. In: K. Aida., K. Tuskamoto and K. Yamauchi (eds.), Eel Biology, pp. 427-434. Springer Verlag, Tokyo.

Tamura, S., T. Shimuza and S. Ikegami. – 1993. Endocytosis in adult eel intestine: Immulogical detection of phagocytic cells in the surface epithelium. Biol. Bull., 184: 330-337. doi:10.2307/1542451

Turner, J.T. –1984. Zooplankton feeding ecology: contents of fecal pellets of the copepods Eucalanus pileatus and Paracalanus Quasimodo from continental shelf water of the Gulf of Mexico. Mar. Ecol. Prog. Ser., 15: 27-46. doi:10.3354/meps015027




Copyright (c) 2010 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es