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Ciliate epibiont effects on feeding, energy reserves, and sensitivity to hydrocarbon contaminants in an estuarine harpacticoid copepod

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Abstract

Although epibiotic protozoans are commonly observed on the chitinous exoskeleton of aquatic crustaceans, relatively little is known about their ecological significance. The significance of protozoan epibionts on benthic copepods has never been examined.Coullana sp., a meiobenthic harpacticoid copepod, is abundant in Louisiana salt marshes and has high incidence (∼50%) of ciliate epibionts. Field and laboratory grazing experiments indicated that ciliate epibionts did not hinderCoullana feeding on benthic or planktonic algae. Contrary to expectations,Coullana with high levels of ciliate epibionts (>8 ind−1) grazed at a significantly higher rate on14C-labeled benthic diatoms added to intact sediment cores than didCoullana with no epibionts.Coullana neutral lipids (examined using Nile Red, a hydrophobic fluorophore) were not significantly influenced by the presence of ciliate epibionts, suggesting that copepods are able to compensate for any additional energetic demands imposed by epibionts. Epibiont effects onCoullana susceptibility to hydrocarbon contaminants were measured by examining survivorship in diesel-spiked sediments. The presence of ciliate epibionts significantly decreased survivorship at relatively low PAH concentrations (12.8 ppm). While ciliate epibionts onCoullana do not dramatically alter total food acquisition or energy storage, they may cause stress, which in turn makesCoullana more susceptible to contaminants and possibly other natural stressors such as food limitation.

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Literature Cited

  • Al-Dhaheri, R. S. andR. L. Willey. 1996. Colonization and reproduction of the epibiotic flagellateColacium vesiculosum (Euglenophyceae) onDaphnia pulex.Journal of Phycology 32: 770–774.

    Article  Google Scholar 

  • Buffan-Dubau, E. andK. R. Carman. 2000a. Diel feeding behavior of meiofauna and their relationships with microalgal resources.Limnology and Oceanography 45:381–395.

    CAS  Google Scholar 

  • Buffan-Dubau, E. andK. R. Carman. 2000b. Extraction of benthic microalgal pigments for HPLC analyses.Marine Ecology Progress Series 204:293–297.

    Article  CAS  Google Scholar 

  • Carman, K. R. andF. C. Dobbs. 1997. Epibiotic microorganisms on copepods and other marine crustaceans.Microscopy Research and Technique 37:116–135.

    Article  CAS  Google Scholar 

  • Carman, K. R., J. W. Fleeger, J. C. Means, S. M. Pomarico, andD. J. McMillin. 1995. Experimental investigation of the effects of polynuclear aromatic hydrocarbons on an estuarine sediment food web.Marine Environmental Research 40:289–318.

    Article  CAS  Google Scholar 

  • Carman, K. C., J. W. Fleeger, andS. M. Pomarico. 1997. Response of a benthic food web to hydrocarbon contamination.Limnology and Oceanography 42:561–571.

    CAS  Google Scholar 

  • Carman, K. C., J. W. Fleeger, andS. M. Pomarico. 2000. Does historical exposure to hydrocarbon contamination alter the response of benthic communities to diesel contamination?Marine Environmental Research 49:255–278.

    Article  CAS  Google Scholar 

  • Carman, K. R., D. Thistle, S. C. Ertman, andM. Foy. 1991. Nile red as a probe for lipid-storage products in benthic copepods.Marine Ecology Progress Series 74:307–311.

    Article  CAS  Google Scholar 

  • Carman, K. R. andM. A. Todaro. 1996. Influence of polycyclic aromatic hydrocarbons on the meiobenthic-copepod community of a Louisiana salt marsh.Journal of Experimental Marine Biology and Ecology 198:37–54.

    Article  CAS  Google Scholar 

  • Chandler, G. T. 1986. High-density culture of meiobenthic harpacticoid copepods within a muddy sediment substrate.Canadian Journal of Fisheries and Aquatic Science 43:53–59.

    Google Scholar 

  • Chandler, G. T. andJ. W. Fleeger. 1983. Meiofaunal colonization of azoic estuarine sediment in Louisiana: Mechanisms of dispersal.Journal of Experimental Marine Biology and Ecology 69:175–188.

    Article  Google Scholar 

  • Chandler, G. T. andJ. W. Fleeger. 1987. Faciltative and inhibitory interactions among estuarine meiobenthic harpacticoid copepods.Ecology 68:1906–1919.

    Article  Google Scholar 

  • Corliss, J. O. 1979. The Ciliated Protozoa: Characterization, Classification and Guide to the Literature. Pergamon Press, New York.

    Google Scholar 

  • Daro, M. H. 1978. A simplified14C method for grazing measurements on natural planktonic populations.Helgolander Meeresuntersuchugen 31:241–248.

    Article  Google Scholar 

  • Daskalakis, K. D. andT. P. O'Connor. 1995. Distribution of chemical concentrations in US coastal and estuarine sediment.Marine Environmental Research 40:381–398.

    Article  CAS  Google Scholar 

  • Decho, A. W. 1986. Water-cover influences on diatom ingestion rates by meiobenthic copepods.Marine Ecology Progress Series 33:139–146.

    Article  Google Scholar 

  • Decho, A. W. 1988. How do harpacticoid grazing rates differ over a tidal cycle? Field verification using chlorophyll-pigment analyses.Marine Ecology Progress Series 45:263–270.

    Article  Google Scholar 

  • Decho, A. W. andJ. W. Fleeger. 1988. Microscale dispersion of meiobenthic copepods in response to food-resource patchiness.Journal of Experimental Marine Biology and Ecology 118:229–241.

    Article  Google Scholar 

  • Felgenhauer, B. E. 1987. Techniques for preparing crustaceans for scanning electron microscopy.Journal of Crustacean Biology 7:71–76.

    Article  Google Scholar 

  • Fernández-Leborans, G., M. J. H. Cordoba, andP. G. del Arco. 1997. Distribution of ciliate epibionts on the portunid crabLiocarcinus depurator (Decapoda: Brachyura).American Microscopy Society 116:171–177.

    Google Scholar 

  • Gee, J. M. 1989. An ecological and economic review of meiofauna as food for fish.Zoological Journal of the Linnean Society 96:243–261.

    Article  Google Scholar 

  • Guillard, R. R. andJ. H. Ryther. 1962. Studies of marine planktonic diatoms. I.Cyclotella nana Hustedt, andDetonula confervacea (Cleve) Gran.Canadian Journal of Microbiology 8: 229–239.

    Article  CAS  Google Scholar 

  • Harrison, P. J., R. E. Waters, andF. J. R. Taylor. 1980. A broad-spectrum artificial seawater medium for coastal and open phytoplankton.Journal Phycology 16:28–35.

    Google Scholar 

  • Herman, S. S. andJ. A. Mihursky. 1964. Infestation of the copepodAcartia tonsa with the stalked ciliateZoothamnium.Science 146:543–544.

    Article  CAS  Google Scholar 

  • Hicks, G. R. F. andB. C. Coull. 1983. The ecology of marine meiobenthic harpacticoid copepods.Oceanography and Marine Biology Annual Review 21:67–175.

    Google Scholar 

  • Hites, R. A., R. E. Laflamme, andJ. G. Windsor, Jr. 1980. Polycyclic aromatic hydrocarbons in marine/aquatic sediments: Their ubiquity.Advances in Chemistry Series 185:289–311.

    Article  CAS  Google Scholar 

  • Kankaala, P. andP. Eloranta. 1987. Epizoic ciliates (Vorticella sp.) compete for food with their hostDaphnia longispina in a small polyhumic lake.Oecologia 73:203–206.

    Article  Google Scholar 

  • Kennish, M. J. 1992. Polynuclear aromatic hydrocarbons, p. 133–181.In Ecology of Estuaries: Anthropogenic Effects. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Long, E. R. 1992. Ranges in chemical concentrations in sediments associated with adverse biological effects.Marine Pollution Bulletin 24:38–45.

    Article  CAS  Google Scholar 

  • Long, E. R., D. D. MacDonald, S. L. Smith, andF. D. Calder. 1995. Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments.Environmental Management 19:81–97.

    Article  Google Scholar 

  • Lotufo, G. R. 1998. Lethal and sublethal toxicity of sediment-associated fluoranthene to benthic copepods: Application of the critical-body-residue approach.Aquatic Toxicology 44:17–30.

    Article  CAS  Google Scholar 

  • Lotufo, G. R. andJ. W. Fleeger. 1997. Effects of sediment-associated phenanthrene on survival, development and reproduction of two species of meiobenthic copepods.Marine Ecology Progress Series 151:91–102.

    Article  CAS  Google Scholar 

  • Luoma, S. N. 1996. The developing framework of marine ecotoxicology: Pollutants as a variable in marine ecosystems?Journal of Experimental Marine Biology and Ecology 200:29–55.

    Article  CAS  Google Scholar 

  • McCall, J. N. andJ. W. Fleeger. 1995. Predation by juvenile fish on hyperbenthic meiofauna: A review with data on postlarvalLeiostomus xanthurus.Vie Milieu 45:61–73.

    Google Scholar 

  • Means, J. C. 1998. Compound-specific GC/MS analysis of alkylated and parent polycyclic aromatic hydrocarbons in waters, sediments, and aquatic organisms.Journal of Offshore Analytical Chemistry 81:657–672.

    CAS  Google Scholar 

  • Montagna, P. A. 1984. In situ measurement of meiobenthic grazing rates on sediment bacteria and edaphic diatoms.Marine Ecology Progress Series 18:119–130.

    Article  Google Scholar 

  • Montagna, P. A. 1995. Rates of metazoan meiofaunal microbivory: A review.Vie Milieu 45:1–9.

    Google Scholar 

  • Montagna, P. A., G. F. Blanchard, andA. Dinet. 1995. Effect of production and biomass of intertidal microphytobenthos on meiofaunal grazing rates.Journal of Experimental Marine Biology and Ecology 185:149–165.

    Article  Google Scholar 

  • Nagasawa, S. 1988. The copepodCentropages abdominalis as a carrier of the stalked ciliateZoothamnuim.Hydrobiologia 167/168: 255–258.

    Article  Google Scholar 

  • Pace, M. andK. R. Carman. 1996. Interspecific differences among meiobenthic copepods in the use of microalgal food resources.Marine Ecology Progress Series 143:77–86.

    Article  Google Scholar 

  • Sherman, K. andE. G. Schaner. 1965.Paracineta sp., an epizoic suctorian found on Gulf of Maine Copepoda.Journal of Protozoology 12:618–625.

    Google Scholar 

  • Small, E. B. andD. H. Lynn. 1985. Phylum Ciliophora, p. 393–575.In J. J. Lee, S. H. Hunter, and E. C. Bovee (eds.), An Illustrated Guide to the Protozoa. Allen Press, Inc., Lawrence, Kansas.

    Google Scholar 

  • Souza-Santos, L. P., J. Castel, andP. J. P. dos Santos. 1995. Feeding rate cycle of the epibenthic harpacticoid copepodHarpacticus flexus: Laboratory experiments using fecal pellet counts.Vie Milieu 45:75–83.

    Google Scholar 

  • Underwood, A. J. 1981. Techniques of analysis of variance in experimental marine biology and ecology.Oceanography and Marine Biology Annual Review 19:513–605.

    Google Scholar 

  • Weissman, P., D. J. Lonsdale, andJ. Yen. 1993. The effect of peritrich ciliates on the production ofAcartia hudsonica in Long Island Sound.Limnology and Oceanography 38:613–622.

    Article  Google Scholar 

  • White, D. C., W. M. Davis, J. S. Nickels, J. D. King, andR. J. Bobbie. 1979. Determination of sedimentary lipid phosphate.Oecologia 40:51–62.

    Article  Google Scholar 

  • Wright, S. W., S. W. Jeffrey, R. F. C. Mantoura, C. C. Llewellyn, T. Bjornland, D. Repeta, andN. Welschmeyer. 1991. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton.Marine Ecology Progress Series 77:183–196.

    Article  CAS  Google Scholar 

  • Xu, Z. andC. W. Burns. 1991. Effects of the epizoic ciliate,Epistylus daphniae, on growth, reproduction and mortality ofBoeckella triarticulata (Thomson) (Copepoda: Calanoida).Hydrobiologia 209:183–189.

    Article  Google Scholar 

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Puckett, G.L., Carman, K.R. Ciliate epibiont effects on feeding, energy reserves, and sensitivity to hydrocarbon contaminants in an estuarine harpacticoid copepod. Estuaries 25, 372–381 (2002). https://doi.org/10.1007/BF02695980

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