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Journal of Parasitology

Published by: American Society of Parasitologists

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Journal of Parasitology 97(5):755-759. 2011
doi: http://dx.doi.org/10.1645/GE-2749.1

Polypocephalus sp. Infects the Nervous System and Increases Activity of Commercially Harvested White Shrimp (Litopenaeus setiferus)

Nadia Carreon, Zen Faulkes, and Brian L. Fredensborg

Department of Biology and Center for Subtropical Studies, The University of Texas-Pan American, 1201 West University Drive, Edinburg, Texas 78539. e-mail: blfredenbor@utpa.edu

abstract:

Larval tapeworms (Polypocephalus sp.) reside within the central nervous system of decapod crustaceans. Living within the nervous system would seem to create an excellent opportunity for the parasites to manipulate the behavior of their hosts, so we tested the hypothesis that behavior of white shrimp (Litopenaeus setiferus) would be correlated with the level of parasitic infection. We videorecorded the behavior of L. setiferus for 8 hr, then examined the nervous system and digestive glands for parasite infection. Larval Polypocephalus sp. were found in the nerve cord, often in large numbers, but only very rarely in the digestive gland, which was typically infected by the larval stage of the nematode, Hysterothylacium sp. There were significantly more Polypocephalus larvae in the abdominal and thoracic ganglia than the subesophageal ganglia and brain. Walking, but not swimming, was significantly and positively related to the number of Polypocephalus sp. lodged in nervous tissue, as well as shrimp carapace length. Polypocephalus sp. is 1 of only a few parasites residing inside the host nervous system and it may, therefore, be suitable for investigating mechanisms of parasite manipulation of invertebrate host behavior.

Received: January 10, 2011; Revised: March 23, 2011; Accepted: March 28, 2011

LITERATURE CITED

Acevedo, L. D., W. M. Hall, and B. Mulloney. 1994. Proctolin and excitation of the crayfish swimmeret system. Journal of Comparative Neurology 345: 612–627.

Antonsen, B. L., and D. H. Edwards. 2007. Mechanisms of serotonergic facilitation of a command neuron. Journal of Neurophysiology 98: 3494–3504.

Arnott, S. A., D. M. Neil, and A. D. Ansell. 1998. Tail-flip mechanism and size-dependent kinematics of escape swimming in the brown shrimp Crangon crangon. Journal of Experimental Biology 201: 1771–1784.

Arnott, S. A., D. M. Neil, and A. D. Ansell. 1999. Escape trajectories of the brown shrimp Crangon crangon, and a theoretical consideration of initial escape angles from predators. Journal of Experimental Biology 202: 193–209.

Caira, J. N., K. Jensen, and C. J. Healy. 1999. On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology 42: 77–151.

Call, G. 2007. A survey of the tapeworm fauna of the cownose ray, Rhinoptera bonasus, from the northern Gulf of Mexico with comments on intermediate hosts. M.A. Thesis. University of Kansas, Lawrence, Kansas, 141 p.

Davis, W. J. 1969. The neural control of swimmeret beating in the lobster. Journal of Experimental Biology 50: 99–117.

Edwards, D. H., W. J. Heitler, and F. B. Krasne. 1999. Fifty years of a command neuron: The neurobiology of escape behavior in the crayfish. Trends in Neurosciences 22: 153–160.

Edwards, D. H., S. R. Yeh, B. E. Musolf, B. L. Antonsen, and F. B. Krasne. 2002. Metamodulation of the crayfish escape circuit. Brain, Behavior and Evolution 60: 360–369.

Eldred, B., R. M. Ingle, K. D. Woodburn, R. F. Hutton, and H. Jones. 1961. Biological observations on the commercial shrimp Penaeus duorarum Burkenroad, in Florida waters. Florida State Board of Conservation Professional Papers Series 3: 1–139.

Faulkes, Z. 2007. The key deletion of an adaptive neural circuit in decapod crustaceans. Brain, Behavior and Evolution 70: 207.

Fuss, C. M., Jr. 1964. Observations on burrowing behavior of the pink shrimp, Penaeus duorarum Burkenroad. Bulletin of Marine Science, Gulf and Caribbean 14: 62–73.

Gilliam, D., and K. M. Sullivan. 1993. Diet and feeding habits of the southern stingray Dasyatis americana in the central Bahamas. Bulletin of Marine Science 52: 1007–1013.

Helluy, S., and F. Thomas. 2003. Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proceedings of the Royal Society of London. Series B: Biological Sciences 270: 563–568.

Jakobsen, P. J., and C. Wedekind. 1998. Copepod reaction to odor stimuli influenced by cestode infection. Behavioral Ecology 9: 414–418.

Krasne, F. B., and D. H. Edwards. 2002. Crayfish escape behavior: Lessons learned. In Crustacean experimental systems in neurobiology, K. Wiese (ed.). Springer-Verlag, Berlin, Germany, p. 3–22.

Lafferty, K. D. 1999. The evolution of trophic transmission. Parasitology Today 15: 111–115.

Lafferty, K. D., and A. K. Morris. 1996. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77: 1390–1397.

Moore, J. 2002. Parasites and the behavior of animals. Oxford University Press, Oxford, U.K., p. 1–338.

Mulloney, B., L. D. Acevedo, and A. G. Bradbury. 1987. Modulation of the crayfish swimmeret rhythm by octopamine and the neuropeptide proctolin. Journal of Neurophysiology 58: 584–597.

Paul, D. H., and B. Mulloney. 1986. Intersegmental coordination of swimmeret rhythms in isolated nerve cords of crayfish. Journal of Comparative Physiology A 158: 215–224.

Pinn, E. H., and A. D. Ansell. 1993. The effect of particle size on the burying ability of the brown shrimp Crangon crangon. Journal of the Marine Biological Association of the United Kingdom 73: 365–377.

Poulin, R., M. A. Curtis, and M. E. Rau. 1992. Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105: 265–271.

Raz-Guzman, A., and L. Huidobro. 2002. Fish communities in two environmentally different estuarine systems of Mexico. Journal of Fish Biology 61: 182–195.

Shaw, J. C., W. J. Korzan, R. E. Carpenter, A. M. Kuris, K. D. Lafferty, C. H. Summers, and Ø. verli. 2009. Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proceedings of the Royal Society B: Biological Sciences 276: 1137–1146.

Shields, J. D. 1992. Parasites and symbionts of the crab Portunus pelagicus from Moreton Bay, Eastern Australia. Journal of Crustacean Biology 12: 94–100.

Skinner, F. K., N. Kopell, and B. Mulloney. 1997. How does the crayfish swimmeret system work? Insights from nearest-neighbor coupled oscillator models. Journal of Computational Neuroscience 4: 151–160.

Smarandache, C., W. M. Hall, and B. Mulloney. 2009. Coordination of rhythmic motor activity by gradients of synaptic strength in a neural circuit that couples modular neural oscillators. Journal of Neuroscience 29: 9351–9360.

Sparks, A. K., and C. T. Fontaine. 1973. Host response in the white shrimp, Penaeus setiferus, to infection by the larval trypanorhynchid cestode, Prochristianella penaei. Journal of Invertebrate Pathology 22: 213–219.

Teshiba, T., A. Shamsian, B. Yashar, S. R. Yeh, D. H. Edwards, and F. B. Krasne. 2001. Dual and opposing modulatory effects of serotonin on crayfish lateral giant escape command neurons. Journal of Neuroscience 21: 4523–4529.

Tripp, M. R., and R. M. Turner. 1983. Helminth infections of some invertebrates of the Georgia Bight. Journal of Invertebrate Pathology 41: 57–67.

Tschuluun, N., W. M. Hall, and B. Mulloney. 2009. State-changes in the swimmeret system: A neural circuit that drives locomotion. Journal of Experimental Biology 212: 3605–3611.

Wiese, K. 2002a. Crustacean experimental systems in neurobiology. Springer-Verlag, Berlin, Germany, 301 p.

Wiese, K. 2002b. The crustacean nervous system. Springer-Verlag, Berlin, Germany, 623 p.

Wine, J. J. 1984. The structural basis of an innate behavioural pattern. Journal of Experimental Biology 112: 283–319.