Intensity-dependent host mortality: What can it tell us about larval growth strategies in complex life cycle helminths?

Parasitology

Volumn 138, Issue 7, 2011, Pages 913-925

  Benesh, D P ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

crowding effect; growth cost; life history strategy; Macrocyclops albidus; Nematoda; resource constraint; virulence

Indexed keywords

ARTICLE; CAMALLANUS LACUSTRIS; COPEPOD; LARVAL DEVELOPMENT; MORTALITY; NEMATODE; NEMATODE LIFE CYCLE STAGE; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL;

ANIMALS; COPEPODA; FEMALE; HOST-PARASITE INTERACTIONS; LARVA; LIFE CYCLE STAGES; MALE; NEMATODA; REGRESSION ANALYSIS; SURVIVAL ANALYSIS;

CAMALLANUS LACUSTRIS; COPEPODA; MACROCYCLOPS ALBIDUS; NEMATODA; VERMES;

EID: 79958831714     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011000370     Document Type: Article

References (85)

1. Abrams, P. A., Leimar, O., Nylin, S. and Wiklund, C. (1996). The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. American Naturalist 147, 381-395.
2. Amin, O. M., Burns, L. A. and Redlin, M. J. (1980). Ecology of Acanthocephalus parksidei Amin, 1975 (Acanthocephala, Echinorhynchidae) in its isopod intermediate host. Proceedings of the Helminthological Society of Washington 47, 37-46.
3. Andersen, P. K. (1991). Survival analysis 1982-1991 - the 2nd decade of the proportional hazards regression-model. Statistics in Medicine 10, 1931-1941.
4. Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission, CABI, Wallingford, UK.
5. Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions I. Regulatory processes. Journal of Animal Ecology 47, 219-247.
6. Awachie, J. B. E. (1966). The development and life-history of Echinorhynchus truttae Schrank 1788 (Acanthocephala). Journal of Helminthology 40, 11-32.
7. Ball, M. A., Parker, G. A. and Chubb, J. C. (2008). The evolution of complex life cycles when parasite mortality is size- or time-dependent. Journal of Theoretical Biology 253, 202-214.
8. Bates, A. E., Poulin, R. and Lamare, M. D. (2010). Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history. Oecologia 163, 651-659.
9. Benesh, D. P. (2010a). Developmental inflexibility of larval tapeworms in response to resource variation. International Journal for Parasitology 40, 487-497.
10. Benesh, D. P. (2010b). What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162, 599-608.
11. Benesh, D. P., Chubb, J. C. and Parker, G. A. (2011). Exploitation of the same trophic link favors convergence of larval life history strategies in complex life cycle helminths. Evolution (in the Press).
12. Benesh, D. P. and Valtonen, E. T. (2007). Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies. Journal of Parasitology 93, 735-741.
13. Brattey, J. (1986). Life-history and population biology of larval Acanthocephalus lucii (Acanthocephala, Echinorhynchidae) in the isopod Asellus aquaticus. Journal of Parasitology 72, 633-645.
14. Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668-672. (Pubitemid 37151562)
15. Brown, S. P., Loot, G., Grenfell, B. T. and Guegan, J. F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519-529.
16. Calentine, R. L. (1965). Biology and taxonomy of Biacetabulum (Cestoda: Caryophyllaeidae). Journal of Parasitology 51, 243-248.
17. Cawthorn, R. J. and Anderson, R. C. (1976). Effects of age, temperature, and previous infection on the development of Physaloptera maxillaris (Nematoda: Physalopteroidea) in field crickets (Acheta pennsylvanicus). Canadian Journal of Zoology 54, 442-448.
18. Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172-181.
19. Chubb, J. C., Ball, M. A. and Parker, G. A. (2010). Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends in Parasitology 26, 93-102.
20. Cornet, S. (2011). Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis. Parasitology 138, 257-265.
21. Courtney, C. C. and Christensen, B. M. (1987). Host-parasite relationships of caryophyllaeid cestodes and aquatic oligochaetes I. Host longevity and parasite intensity. Journal of Parasitology 73, 1124-1132.
22. Crofton, H. D. (1971). Quantitative approach to parasitism. Parasitology 62, 179-193.
23. Day, T. (2003). Virulence evolution and the timing of disease life-history events. Trends in Ecology and Evolution 18, 113-118.
24. Day, T. and Rowe, L. (2002). Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. American Naturalist 159, 338-350. (Pubitemid 34243650)
25. Denny, M. (1969). Life-cycles of helminth parasites using Gammarus lacustris as an intermediate host in a Canadian lake. Parasitology 59, 795-827.
26. Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483-489. (Pubitemid 32281104)
27. Duclos, L. M., Danner, B. J. and Nickol, B. B. (2006). Virulence of Corynosoma constrictum (Acanthocephala: Polymorphidae) in Hyalella azteca (Amphipoda) throughout parasite ontogeny. Journal of Parasitology 92, 749-755.
28. Ferreira, S. M., Jensen, K. T., Martins, P., Sousa, S. F., Marques, J. C. and Pardal, M. A. (2005). Impact of microphallid trematodes on the survivorship, growth, and reproduction of an isopod (Cyathura carinata). Journal of Experimental Marine Biology and Ecology 318, 191-199.
29. Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253-265. (Pubitemid 39290143)
30. Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061-1070.
31. Freeman, R. S. (1952). Temperature as a factor affecting development of Monoecocestus (Cestoda: Anoplocephalidae) in oribatid mites. Experimental Parasitology 1, 256-262.
32. Gandon, S. (2004). Evolution of multihost parasites. Evolution 58, 455-469.
33. Gotthard, K. (2001). Growth strategies of ectothermic animals in temperate environments. In Environment and Animal Development (ed. Thorndyke, D. A. M.), pp. 287-304. BIOS Scientific Publishers, Oxford , UK.
34. Guinnee, M. A. and Moore, J. (2004). The effect of parasitism on host fecundity is dependent on temperature in a cockroach-acanthocephalan system. Journal of Parasitology 90, 673-677. (Pubitemid 39128715)
35. Hansen, E. K. and Poulin, R. (2005). Impact of a microphallid trematode on the behaviour and survival of its isopod intermediate host: phylogenetic inheritance? Parasitology Research 97, 242-246.
36. Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The "crowding effect" in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302-307. (Pubitemid 34493398)
37. Heins, D. C., Birden, E. L. and Baker, J. A. (2010). Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus. Parasitology 137, 1681-1686.
38. Huizinga, H. W. (1967). The life cycle of Contracaecum multipapillatum (Von Drasche, 1882) Lucker, 1941 (Nematoda: Heterochelidae). The Journal of Parasitology 53, 368-375.
39. Hurd, H., Warr, E. and Polwart, A. (2001). A parasite that increases host lifespan. Proceedings of the Royal Society of London, B 268, 1749-1753. (Pubitemid 32758613)
40. Iwasa, Y. and Wada, G. (2006). Complex life cycle and body sizes at life-history transitions for macroparasites. Evolutionary Ecology Research 8, 1427-1443. (Pubitemid 46032552)
41. Keymer, A. E. (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405-421.
42. Kisielewska, K. (1959). Types of Copepoda and Drepanidotaenia lanceolata (Bloch) host-parasite systems established experimentally. Acta Parasitologica Polonica 7, 371-392.
43. Kokkotis, T. and McLaughlin, J. D. (2006). Pathogenicity of the hymenolepidid cestode Microsomacanthus hopkinsi in its intermediate host, Hyalella azteca: implications for transmission, host fitness, and host populations. Canadian Journal of Zoology 84, 32-41.
44. Korting, W. (1975). Larval development of Bothriocephalus sp (Cestoda: Pseudophyllidea) from carp (Cyprinus carpio L.) in Germany. Journal of Fish Biology 7, 727-733.
45. Lagrue, C. and Poulin, R. (2008). Intra-and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435-1444.
46. Latham, A. D. M. and Poulin, R. (2002). Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Marine Biology 141, 1131-1139. (Pubitemid 36128313)
47. Lopez, C., Panadero, R., Diez, P. and Morrondo, P. (1998). Effect of the infection by Neostrongylus linearis on the survival of the intermediate host Cernuella (cernuella) virgata. Parasite 5, 181-184. (Pubitemid 128505057)
48. Measures, L. N. (1988). The development of Eustrongylides tubifex (Nematoda, Dioctophymatoidea) in oligochaetes. Journal of Parasitology 74, 294-304.
49. Meissner, K. and Bick, A. (1999). Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae) - laboratory studies. Diseases of Aquatic Organisms 35, 47-52. (Pubitemid 29073175)
50. Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends in Ecology and Evolution 16, 254-260. (Pubitemid 32288153)
51. Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 39-57.
52. Moravec, F. (1978). The development of the nematode Philometra obturans (Prenant, 1886) in the intermediate host. Folia Parasitologica 25, 303-315.
53. Moravec, F. (1969). Observations on the development of Camallanus lacustris (Zoega, 1776). Vèstnik Ceskoslovenské Zoologické Spolecnosti 33, 15-33.
54. Nie, P. and Kennedy, C. R. (1993). Infection dynamics of larval Bothriocephalus claviceps in Cyclops vicinus. Parasitology 106, 503-509.
55. Okaka, C. E. (1989). Studies on the development of the oncosphere and procercoid of Cyathocephalus truncatus (Cestoda) in the intermediate host, Gammarus pulex. Zoologica Scripta 18, 205-209.
56. Outreman, Y., Cezilly, F. and Bollache, L. (2007). Field evidence of host size-dependent parasitism in two manipulative parasites. Journal of Parasitology 93, 750-754. (Pubitemid 47502185)
57. Parker, G. A., Ball, M. A. and Chubb, J. C. (2009a). To grow or not to grow? Intermediate and paratenic hosts as helminth life cycle strategies. Journal of Theoretical Biology 258, 135-147.
58. Parker, G. A., Ball, M. A. and Chubb, J. C. (2009b). Why do larval helminths avoid the gut of intermediate hosts? Journal of Theoretical Biology 260, 460-473.
59. Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003a). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480-484. (Pubitemid 37237037)
60. Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003b). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 47-54. (Pubitemid 36108130)
61. Pilecka-Rapacz, M. (1986). On the development of acanthocephalans of the genus Acanthocephalus Koelreuther, 1771, with special attention to their influence on intermediate host, Asellus aquaticus L. Acta Parasitologica Polonica 30, 233-250.
62. Ponton, F., Lalubin, F., Fromont, C., Wilson, K., Behm, C. and Simpson, S. J. (2011). Hosts use altered macronutrient intake to circumvent parasite-induced reduction in fecundity. International Journal for Parasitology 41, 43-50.
63. Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.
64. Poulin, R., Curtis, M. A. and Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behavior of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265-271.
65. Poulin, R. and Latham, A. D. M. (2003). Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574-581.
66. Poulin, R., Nichol, K. and Latham, A. D. A. (2003). Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425-433.
67. Robert, F. and Gabrion, C. (1991). Experimental approach to the specificity in first intermediate hosts of Bothriocephalids (Cestoda, Pseudophyllidea) from marine fish. Acta Oecologica 12, 617-632.
68. Rosen, L., Ash, L. R. and Wallace, G. D. (1970). Life history of canine lungworm Angiostrongylus vasorum (Baillet). American Journal of Veterinary Research 31, 131-139.
69. Rosen, R. and Dick, T. A. (1983). Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Canadian Journal of Zoology 61, 2120-2128.
70. Sakanari, J. and Moser, M. (1985). Salinity and temperature effects on the eggs, coracidia, and procercoids of Lacistorhynchus tenuis (Cestoda, Trypanorhyncha) and induced mortality in a first intermediate host. Journal of Parasitology 71, 583-587.
71. Saldanha, I., Leung, T. L. F. and Poulin, R. (2009). Causes of intraspecific variation in body size among trematode metacercariae. Journal of Helminthology 83, 289-293.
72. Sandland, G. J. and Goater, C. P. (2000). Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 1056-1060.
73. Shostak, A. W., Rosen, R. B. and Dick, T. A. (1985). The use of growthcurves to assess the crowding effect on procercoids of the tapeworm Triaenophorus crassus in the copepod host Cyclops bicuspidatus thomasi. Canadian Journal of Zoology 63, 2343-2351.
74. Shostak, A. W., Walsh, J. G. and Wong, Y. C. (2008). Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 1019-1033.
75. Skorping, A. (1984). Density-dependent effects in a parasitic nematode, Elaphostrongylus rangiferi, in the snail intermediate host. Oecologia 64, 34-40.
76. Skorping, A. (1985). Parasite-induced reduction in host survival and fecundity - the effect of the nematode Elaphostrongylus rangiferi on the snail intermediate host. Parasitology 91, 555-562.
77. Solomon, A., Paperna, I. and Alkon, P. U. (1996). The suitability of Trochoidea seetzenii of different ages as snail intermediate hosts of Muellerius cf. capillaris (Nematoda: Protostrongylidae). International Journal for Parasitology 26, 1317-1319.
78. Steinauer, M. L. and Nickol, B. B. (2003). Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251-254.
79. Thomas, F., Renaud, F., Rousset, F., Cezilly, F. and Demeeus, T. (1995). Differential mortality of two closely-related host species induced by one parasite. Proceedings of the Royal Society of London, B 260, 349-352. (Pubitemid 26450058)
80. Trowe, S. (1997). Morphometrical differentiation of Anoplocephalidae cysticeroids with a contribution to reproduction of oribatid mites experimentally infected. Ph.D. thesis, Freie Universität Berlin, Germany.
81. Uznanski, R. L. and Nickol, B. B. (1980). Parasite population regulation: lethal and sublethal effects of Leptorhynchoides thecatus (Acanthocephala, Rhadinorhynchidae) on Hyalella azteca (Amphipoda). Journal of Parasitology 66, 121-126.
82. Valkounova, J. (1980). The most important factors affecting the larval development of cestodes of the family Hymenolepididae in crustaceans (Copepoda). Vèstnik Ceskoslovenské Zoologické Spolecnosti 44, 230-240.
83. Van der Veen, I. T. and Kurtz, J. (2002). To avoid or eliminate: cestode infections in copepods. Parasitology 124, 465-474.
84. Werner, E. E. and Gilliam, J. F. (1984). The ontogenetic niche and species interactions in size structured populations. Annual Review of Ecology and Systematics 15, 393-425.
85. Wootten, R. (1974). Studies on the life history and development of Proteocephalus percae (Müller) (Cestoda: Proteocephalidea). Journal of Helminthology 48, 269-281.