Host-parasite interactions and competition between tubificid species in a benthic community

Freshwater Biology

Volumn 54, Issue 8, 2009, Pages 1616-1628

  Elwell, L C Steinbach ^a   Kerans, B L ^a   Zickovich, J ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Community ecology; Dilution effect; Limnodrilus hoffmeisteri; Myxobolus cerebralis; Tubifex tubifex

Indexed keywords

BACTERIA (MICROORGANISMS); LIMNODRILUS HOFFMEISTERI; MYXOBOLUS CEREBRALIS; MYXOSOMA CEREBRALIS; MYXOZOA; SALMONIDAE; TUBIFEX TUBIFEX; TUBIFICIDAE;

EID: 67650302328     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/j.1365-2427.2009.02211.x     Document Type: Article

References (66)

1. Blazer V.S., Waldrop T.B., Schill W.B., Densmore C.L. Smith D. (2003) Effects of water temperature and substrate type on spore production and release in eastern Tubifex tubifex worms infected with Myxobolus cerebralis. Journal of Parasitology, 89, 21 26. (Pubitemid 36278643)
2. Bonacina C., Bonomi G. Monti C. (1989) Density-dependent processes in cohorts of Tubifex tubifex, with special emphasis on the control of fecundity. Hydrobiologia, 180, 135 141.
3. Bonomi G. Di Cola G. (1980) Population dynamics of Tubifex tubifex, studied by means of a new model. In : Aquatic Oligochaete Biology (Eds R.O. Brinkhurst D.G. Cook) pp. 183 203. Plenum Press, New York.
4. Brinkhurst R.O. (1974) Factors mediating interspecific aggregation of Tubificid oligochaetes. Journal of the Fisheries Research Board of Canada, 31, 460 462.
5. Brinkhurst R.O. Jamieson B.G.M. (1971) Aquatic Oligochaeta of the World. University of Toronto Press, Toronto, ON.
6. Brinkhurst R.O., Chua K.E. Kaushik N.K. (1972) Interspecific interactions and selective feeding by tubificid oligochaetes. Limnology and Oceanography, 17, 122 132.
7. Calabrese E.J. Baldwin L.A. (2003) Toxicology rethinks its central belief. Nature, 421, 691 692. (Pubitemid 36227604)
8. Dobson A. (2004) Population dynamics of pathogens with multiple host species. American Naturalist, 164, S64 S78.
9. Dobson A. Crawley M. (1994) Pathogens and the structure of plant communities. Trends in Ecology and Evolution, 9, 393 398. (Pubitemid 124001483)
10. Dobson A.P. Hudson P.J. (1986) Parasites, disease and the structure of ecological communities. Trends in Ecology and Evolution, 1, 11 15.
11. Ebert D. Mangin K.L. (1997) The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution, 51, 1828 1837. (Pubitemid 28104543)
12. Ebert D., Zschokke-Rohringer C.D. Carius H.J. (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasiite Pasteuria ramosa. Proceeding of the Royal Society of London B, 265, 2127 2134. (Pubitemid 28502550)
13. Ebert D., Zschokke-Rohringer C.D. Carius H.J. (2000) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia, 122, 200 209. (Pubitemid 30096238)
14. El-Matbouli M., Hoffmann R.W. Mandok C. (1995) Light and electron microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. Journal of Fish Biology, 46, 919 935.
15. El-Matbouli M., Gay M., McDowell T.S., Georgiadis M.P. Hedrick R.P. (1999a) The potential for using biological control technologies in the management of whirling disease. In : Proceedings of the 5th Annual Whirling Disease Symposium, pp. 191 196. Missoula, Montana, 18-20 February 1999. Whirling Disease Foundation, Bozeman, MT.
16. El-Matbouli M., McDowell T.S., Antonio D.B., Andree K.B. Hedrick R.P. (1999b) Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. International Journal of Parasitology, 29, 627 641. (Pubitemid 29225138)
17. Ezenwa V.O., Godsey M.S., King R.J. Guptill S.G. (2006) Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proceedings of the Royal Society B, 273, 109 117. (Pubitemid 46768052)
18. Freeland W.J. (1983) Parasites and the coexistence of animal host species. American Naturalist, 121, 223 236. (Pubitemid 14271076)
19. Gilbert M.A. Granath W.O. Jr. (2001) Persistent infection of Myxobolus cerebralis, the causative agent of salmonids whirling disease, in Tubifex tubifex. Journal of Pararsitology, 87, 101 107. (Pubitemid 32172350)
20. Goldberg D.E. Scheiner S.M. (2001) ANOVA and ANCOVA-field competition experiments. In : Design and Analysis of Ecological Experiments, 2nd edn (Eds S.M. Scheiner J. Gurevitch pp. 77 98. Oxford University Press, Oxford.
21. Grosholz E.D. (1992) Interactions of intraspecific, interspecific and apparent competition with host-pathogen population dynamics. Ecology, 73, 507 514.
22. Hedrick R.P., McDowell T., Mukkatira K., MacConnell E. Petri B. (2008) Effects of freezing, drying, ultraviolet irradiation, chlorine and quaternary ammonium treatments on the infectivity of myxospores of Myxobolus cerebralis for Tubifex tubifex. Journal of Aquatic Animal Health, 20, 116 125.
23. Holt R.D., Dobson A.P., Begon M., Bowers R.G. Schauber E.M. (2003) Parasite establishment in host communities. Ecology Letters, 6, 837 842. (Pubitemid 37105914)
24. Iversen E.S. Kelly J.F. (1976) Microsporidious successfully transmitted experimentally in pink shrimp. Journal of Invertebrate Pathology, 27, 407 408.
25. Kaster J.L. (1980) The reproductive biology of Tubifex tubifex Muller (Annelida: Tubificidae. American Midland Naturalist, 104, 364 366.
26. Kathman R.D. Brinkhurst R.O. (1998) Guide to Freshwater Oligochaetes in North America. Aquatic Resources Center, College Grove.
27. Keesing F., Holt R.D. Ostfeld R.S. (2006) Effects of species diversity on disease risk. Ecology Letter, 9, 485 498.
28. Kerans B.L., Rasmussen C., Stevens R., Colwell A.E. Winton J.R. (2004) Differential propagation of the metazoan parasite Myxobolus cerebralis by Limnodrilus hoffmeisteri, Ilyodrilus templetoni, and genetically distinct strains of Tubifex tubifex. Journal of Parasitology, 6, 1366 1373. (Pubitemid 40389284)
29. Kerans B.L., Stevens R.I. Lemmon J.C. (2005) Water temperature affects a host-parasite interaction: Tubifex tubifex and Myxobolus cerebralis. Journal of Aquatic Animal Health, 17, 216 221. (Pubitemid 41279096)
30. Kopp K. Jokela J. (2007) Resistant invaders can convey benefits to native species. Oikos, 116, 295 301. (Pubitemid 46146504)
31. Kosiorek D. (1974) Development cycle of Tubifex tubifex Mull. in experimental culture. Polskie Archiwum Hydrobiologii, 21, 411 422.
32. Krueger R.C., Kerans B.L., Vincent E.R. Rasmussen C. (2006) Risk of Myxobolus cerebralis infection to rainbow trout in the Madison River, Montana, USA. Ecological Application, 16, 770 783.
33. Lazim M.N. Learner M.A. (1986) The life cycle and productivity of Tubifex tubifex (Oligochaeta: Tubificidae) in the moat-feeder stream, Cardiff, South Wales. Holarctic Ecology, 9, 185 192.
34. Little T.J. Ebert D. (2000) The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics. Proceedings of the Royal Society of London, B, 267, 2037 2042. (Pubitemid 30828827)
35. LoGiudice R., Ostfeld R.S., Schmidt K.A. Keesing F. (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences of the United States of America, 100, 567 571. (Pubitemid 36126092)
36. Markiw M.E. Wolf K. (1983) Myxosoma cerebralis (Myxozoa: Myxosporea), etiological agent of salmonids whirling disease requires tubificid worm (Annelida: Oligochaeta) in its life cycle. Journal of Protozoology, 30, 561 564.
37. McCall P.L. Fisher J.B. (1980) Effects of tubificid oligochaetes on physical and chemical properties of Lake Erie sediments. In : Aquatic Oligochaete Biology (Eds R.O. Brinkhurst D.G. Cook) pp. 253 318. Plenum Press, New York City.
38. Mermillod-Blondin F., Gerinl M., Degrange V., Lensi R., Chasse J., Rard M. Creuze des Chatelliers M. (2001) Testing the functional redundancy of Limnodrilus and Tubifex (Oligochaeta, Tubificidae) in hyporheic sediments: and experimental study in microcosms. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1747 1759. (Pubitemid 33023349)
39. Milbrink G. (1987) Mutualistic relationships between cohabiting tubificid species. Hydrobiologia, 155, 193.
40. Milbrink G. (1993) Evidence for mutualistic interactions in freshwater oligochaete communities. Oikos, 68, 317 322.
41. Minchella D.J. Scott M.E. (1991) Parasitism: a cryptic determinant of animal community structure. Trends in Ecology and Evolution, 6, 250 254. (Pubitemid 121002986)
42. Modin J. (1998) Whirling disease in California: a review of its history, distribution, and impacts, 1965-1997. Journal of Aquatic Animal Health, 10, 132 142. (Pubitemid 28305642)
43. Moore J. (1984) Altered behavioural responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist, 123, 572 577.
44. Mouritsen K.N. Poulin R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology, 124, S101 S117.
45. O'Grodnick J. (1975) Whirling disease concentration using the continuous plankton centrifuge. Journal of Wildlife Diseases, 11, 54 57.
46. Park T. (1948) Experimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium confusum Duvall and Tribolium castaneum Herbst. Ecological Monographs, 18, 267 307.
47. Parsons P.A. (2001) The hormetic zone: an ecological and evolutionary perspective based upon habitat characteristics and fitness selection. Quarterly Review of Biology, 76, 459 467. (Pubitemid 33136535)
48. Pennak R.W. (1978) Fresh-Water Invertebrates of the United States, 2nd edn. John Wiley and Sons, New York.
49. Poddubnaya T.L. (1980) Life cycles of mass species of Tubificidae. In : Aquatic Oligochaete Biology (Eds R.O. Brinkhurst D.G. Cook) pp. 173 184. Plenum Press, New York City.
50. Poulin R. (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology, 10, S109 S118.
51. Price P.W., Westoby M., Rice B., Atsatt P.R., Fritz R.S., Thompson J.N. Mobley K. (1986) Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics, 17, 487 505.
52. Pulkkinen K. (2007) Microparasite transmission to Daphnia magna decreases in the presence of conspecifics. Oecologia, 154, 45 53. (Pubitemid 47583391)
53. Rasmussen C., Zickovich J., Winton J.R. Kerans B.L. (2008) Variability in triactinomyxon production from Tubifex tubifex populations from the same mitochondrial DNA lineage infected with Myxobolus cerebralis, the causative agent of whirling disease in salmonids. Journal of Parasitology, 94, 700 708. (Pubitemid 351999777)
54. Rudolf V.H. Antonovics J. (2005) Species coexistence and pathogens with frequency-dependent transmission. American Naturalist, 166, 112 118. (Pubitemid 40886778)
55. SAS Institute (2001) SAS/STAT for Windows Version 8.1. SAS Institute, Cary, NC.
56. Schmidt K.A. Ostfeld R.S. (2001) Biodiversity and the dilution effect in disease ecology. Ecology, 82, 609 619. (Pubitemid 32175310)
57. Settle W.H. Wilson L.T. (1990) Invasion by the variegated leafhopper and biotic interactions: parasitism, competition and apparent competition. Ecology, 71, 1461 1470.
58. Steinbach Elwell L.C., Kerans B.L., Rasmussen C. Winton J.R. (2006) Interactions among two strains to Tubifex tubifex (Oligochaeta: Tubificidae) and Myxobolus cerebralis (Myxozoa). Diseases of Aquatic Organisms, 68, 121 139.
59. Stevens R., Kerans B.L., Lemmon J.C. Rasmussen C. (2001) The effects of Myxobolus cerebralis myxospore dose on triactinomyxon production and biology of Tubifex tubifex from two geographic regions. Journal of Parasitology, 87, 315 321. (Pubitemid 32303673)
60. Théron A., Gérard C. Moné H. (1992) Early enhanced growth of the digestive gland of Biomphalaria glabrata infected with Schistosoma mansoni: side effect or parasite manipulation? Parasitology Research, 78, 445 450.
61. Thomas F., Guegan J.-F., Michalakis Y. Renaud F. (2000a) Parasites and host life-history traits: implications for community ecology and species co-existence. International Journal of Parasitology, 30, 669 674. (Pubitemid 30209955)
62. Thomas F., Poulin R., Guégan J.-F., Michalakis Y. Renaud F. (2000b) Are there pros and well as cons to being parasitized? Parasitology Today, 16, 533 535.
63. Thompson S.N. Kavaliers M. (1994) Physiological bases for parasite-induced alterations of host behaviour. Parasitology, 109, S119 S138.
64. Wolf K. Markiw M.E. (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science, 225, 365 368.
65. Wolf K., Markiw M.E. Hiltunen J.K. (1986) Salmonid whirling disease: Tubifex tubifex (Müller) identified as the essential oligochaete in the protozoan life cycle. Journal of Fish Diseases, 9, 83 85.
66. Yan G., Stevens L., Goodnight C.J. Schall J.J. (1998) Effects of a tapeworm parasite on the competition of tribolium beetles. Ecology, 79, 1093 1103. (Pubitemid 28378714)