Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host

Parasites and Vectors

Volumn 5, Issue 1, 2012, Pages

  Benesh, Daniel P ^a   Hafer, Nina ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

Cercomer; Cestoda; Complex life cycle; Energy allocation; Glycogen; Life history tradeoff; Metamorphosis; Plerocercoid; Procercoid

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CESTODE; CONTROLLED STUDY; COPEPOD; ENERGY METABOLISM; FEMALE; GROWTH; GROWTH RATE; INTERMEDIATE HOST; LARVAL DEVELOPMENT; LARVAL STAGE; MALE; NONHUMAN; ONTOGENY; SCHISTOCEPHALUS SOLIDUS; STICKLEBACK; ANIMAL; FISH DISEASE; GROWTH, DEVELOPMENT AND AGING; PARASITOLOGY; SMEGMAMORPHA;

ANIMALS; CESTODA; COPEPODA; FISH DISEASES; SMEGMAMORPHA;

EID: 84860592617     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-5-90     Document Type: Article

References (81)

1. Semlitsch RD, Scott DE, Pechmann JHK: Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 1988, 69:184-192.
2. Scott DE: The effect of larval density on adult demographic traits in Ambystoma opacum. Ecology 1994, 75:1383-1396.
3. Paradis AR, Pepin P, Brown JA: Vulnerability of fish eggs and larvae to predation: review of the influence of the relative size of prey and predator. Can J Fish Aquat Sci 1996, 53:1226-1235.
4. Taylor BW, Anderson CR, Peckarsky BL: Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia 1998, 114:494-502.
5. Phillips NE: Effects of nutrition-mediated larval condition on juvenile performance in a marine mussel. Ecology 2002, 83:2562-2574.
6. Altwegg R, Reyer HU: Patterns of natural selection on size at metamorphosis in water frogs. Evolution 2003, 57:872-882.
7. Emlet RB, Sadro SS: Linking stages of life history: how larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula). Integr Comp Biol 2006, 46:334-346.
8. Werner EE, Gilliam JF: The ontogenetic niche and species interactions in size structured populations. Ann Rev Ecol Syst 1984, 15:393-425.
9. Rowe L, Ludwig D: Size and timing of metamorphosis in complex life cycles - time constraints and variation. Ecology 1991, 72:413-427.
10. Abrams PA, Rowe L: The effects of predation on the age and size of maturity of prey. Evolution 1996, 50:1052-1061.
11. Abrams PA, Leimar O, Nylin S, Wiklund C: The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 1996, 147:381-395.
12. Day T, Rowe L: Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 2002, 159:338-350.
13. Berner D, Blanckenhorn WU: An ontogenetic perspective on the relationship between age and size at maturity. Funct Ecol 2007, 21:505-512.
14. Rolff J, Van de Meutter F, Stoks R: Time constraints decouple age and size at maturity and physiological traits. Am Nat 2004, 164:559-565.
15. Campero M, De Block M, Ollevier F, Stoks R: Correcting the short-term effect of food deprivation in a damselfly: mechanisms and costs. J Anim Ecol 2008, 77:66-73.
16. Van Allen BG, Briggs VS, McCoy MW, Vonesh JR: Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs. Oecologia 2010, 164:891-898.
17. Twombly S, Clancy N, Burns CW: Life history consequences of food quality in the freshwater copepod Boeckella triarticulata. Ecology 1998, 79:1711-1724.
18. Dias GM, Marshall DJ: Does the relationship between offspring size and performance change across the life-history? Oikos 2010, 119:154-162.
19. Marshall DJ, Keough MJ: Variable effects of larval size on post-metamorphic performance in the field. Mar Ecol Prog Ser 2004, 279:73-80.
20. Zera AJ, Harshman LG: The physiology of life history trade-offs in animals. Ann Rev Ecol Syst 2001, 32:95-126.
21. Marshall DJ, Pechenik JA, Keough MJ: Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial, ascidian Diplosoma listerianum. Mar Ecol Prog Ser 2003, 246:153-162.
22. Pechenik JA: Larval experience and latent effects - metamorphosis is not a new beginning. Integr Comp Biol 2006, 46:323-333.
23. Slos S, De Meester L, Stoks R: Food level and sex shape predator-induced physiological stress: immune defence and antioxidant defence. Oecologia 2009, 161:461-467.
24. Marden JH, Fescemyer HW, Saastamoinen M, MacFarland SP, Vera JC, Frilander MJ, Hanski I: Weight and nutrition affect pre-mRNA splicing of a muscle gene associated with performance, energetics and life history. J Exp Biol 2008, 211:3653-3660.
25. De Block M, Stoks R: Fitness effects from egg to reproduction: Bridging the life history transition. Ecology 2005, 86:185-197.
26. Stoks R, De Block M, McPeek MA: Physiological costs of compensatory growth in a damselfly. Ecology 2006, 87:1566-1574.
27. Davies CM, Webster JP, Woolhouse MEJ: Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proc R Soc B 2001, 268:251-257.
28. Gower CM, Webster JP: Fitness of indirectly transmitted pathogens: restraint and constraint. Evolution 2004, 58:1178-1184.
29. Hammerschmidt K, Kurtz J: Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proc R Soc B 2005, 272:2511-2518.
30. Walker SM, Hoey E, Fletcher H, Brennan G, Fairweather I, Trudgett A: Stage-specific differences in fecundity over the life-cycle of two characterized isolates of the liver fluke, Fasciola hepatica. Parasitology 2006, 133:209-216.
31. Parker GA, Chubb JC, Roberts GN, Michaud M, Milinski M: Optimal growth strategies of larval helminths in their intermediate hosts. J Evol Biol 2003, 16:47-54.
32. Parker GA, Ball MA, Chubb JC: Why do larval helminths avoid the gut of intermediate hosts? J Theor Biol 2009, 260:460-473.
33. Parker GA, Ball MA, Chubb JC: To grow or not to grow? Intermediate and paratenic hosts as helminth life cycle strategies. J Theor Biol 2009, 258:135-147.
34. Ball MA, Parker GA, Chubb JC: The evolution of complex life cycles when parasite mortality is size- or time-dependent. J Theor Biol 2008, 253:202-214.
35. Iwasa Y, Wada G: Complex life cycle and body sizes at life-history transitions for macroparasites. Evol Ecol Res 2006, 8:1427-1443.
36. Chubb JC, Ball MA, Parker GA: Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends Parasitol 2010, 26:93-102.
37. Rosen R, Dick TA: Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the 1st intermediate host. Can J Zool 1983, 61:2120-2128.
38. Tierney JF, Crompton DWT: Infectivity of plerocercoids of Schistocephalus solidus (Cestoda, Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. J Parasitol 1992, 78:1049-1054.
39. Schärer L, Karlsson LM, Christen M, Wedekind C: Size dependent sex allocation in a simultaneous hermaphrodite parasite. J Evol Biol 2001, 14:55-67.
40. Steinauer ML, Nickol BB: Effect of cystacanth body size on adult success. J Parasitol 2003, 89:251-254.
41. Fredensborg BL, Poulin R: Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? Int J Parasitol 2005, 35:1061-1070.
42. Dörücü M, Wilson D, Barber I: Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks. J Parasitol 2007, 93:1521-1523.
43. Benesh DP, Weinreich F, Kalbe M: The relationship between larval size and fitness in the tapeworm Schistocephalus solidus: bigger is better? Oikos,. in press.
44. Mueller JF: Laboratory propagation of Spirometra mansonoides (Mueller 1935) as an experimental tool. VII. Improved techniques and additional notes on the biology of the cestode. J Parasitol 1966, 52:437-443.
45. Hammerschmidt K, Koch K, Milinski M, Chubb JC, Parker GA: When to go: optimization of host switching in parasites with complex life cycles. Evolution 2009, 63:1976-1986.
46. Gandon S: Evolution of multihost parasites. Evolution 2004, 58:455-469.
47. Parker GA, Chubb JC, Ball MA, Roberts GN: Evolution of complex life cycles in helminth parasites. Nature 2003, 425:480-484.
48. Clarke AS: Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus. Proc Zool Soc Lond 1954, 124:257-302.
49. Dubinina MN: Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Dehli: Amerind Publishing Co. Pvt. Ltd.; 1980.
50. Hammerschmidt K, Kurtz J: Schistocephalus solidus: establishment of tapeworms in sticklebacks - fast food or fast lane? Exp Parasitol 2007, 116:142-149.
51. Barber I, Scharsack JP: The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 2010, 137:411-424.
52. Benesh DP: Developmental inflexibility of larval tapeworms in response to resource variation. Int J Parasitol 2010, 40:487-497.
53. Benesh DP: What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 2010, 162:599-608.
54. Smyth JD: Studies on tapeworm physiology I. the cultivation of Schistocephalus solidus in vitro. J Exp Biol 1946, 23:47-70.
55. Wedekind C: The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitology 1997, 115:317-324.
56. Lüscher A, Milinski M: Simultaneous hermaphrodites reproducing in pairs self-fertilize some of their eggs: an experimental test of predictions of mixed-mating and Hermaphrodite's Dilemma theory. J Evol Biol 2003, 16:1030-1037.
57. Van der Veen IT, Kurtz J: To avoid or eliminate: cestode infections in copepods. Parasitology 2002, 124:465-474.
58. Zander CD, Groenewold S, Strohbach U: Parasite transfer from crustacean to fish hosts in the Lubeck Bight, SW Baltic Sea. Helgolander Meeresun 1994, 48:89-105.
59. Rusinek OT, Bakina MP, Nikolskii AV: Natural infection of the calanoid crustacean Epischura baicalensis by procercoids of Proteocephalus sp in Listvenichnyi Bay, Lake Baikal. J Helminthol 1996, 70:237-247.
60. Dörücü M: Seasonal variation of pseudophyllidean cestode, Diphyllobothrium spp. infection in Cyclops strenuus abyssorum (Copepoda) in Loch Lomond. Turk J Zool 1999, 23:85-92.
61. Hanzelova V, Gerdeaux D: Seasonal occurrence of the tapeworm Proteocephalus longicollis and its transmission from copepod intermediate host to fish. Parasitol Res 2003, 91:130-136.
62. Hanzelova V, Scholz T, Gerdeaux D, Kuchta R: A comparative study of Eubothrium salvelini and E. crassum (Cestoda: Pseudophyllidea) parasites of Arctic charr and brown trout in alpine lakes. Environ Biol Fish 2002, 64:245-256.
63. Smyth JD, McManus DP: The physiology and biochemistry of cestodes. Cambridge: Cambridge University Press; 1989.
64. Wedekind C, Christen M, Schärer L, Treichel N: Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode. Aquat Ecol 2000, 34:279-285.
65. Scharsack JP, Koch K, Hammerschmidt K: Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proc R Soc B 2007, 274:3151-3158.
66. Kalbe M, Eizaguirre C, Dankert I, Reusch TBH, Sommerfeld RD, Wegner KM, Milinski M: Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity. Proc R Soc B 2009, 276:925-934.
67. Gómez-Lechón MJ, Ponsoda X, Castell JV: A microassay for measuring glycogen in 96-well-cultured cells. Anal Biochem 1996, 236:296-301.
68. Roff DA, Fairbairn DJ: The evolution of trade-offs: where are we? J Evol Biol 2007, 20:433-447.
69. Benesh DP, Chubb JC, Parker GA: Exploitation of the same trophic link favors convergence of larval life-history strategies in complex life cycle helminths. Evolution 2011, 65:2286-2299.
70. Frank SA: Models of parasite virulence. Quart Rev Biol 1996, 71:37-78.
71. Combes C: Evolution of parasite life cycles. In Parasite-host associations Coexistence or conflict. Edited by Toft CA, Aeschlimann A, Bolis L. Oxford: Oxford University Press; 1991:62-82.
72. Metcalfe NB, Monaghan P: Compensation for a bad start: grow now, pay later? Trends Ecol Evol 2001, 16:254-260.
73. Crean AJ, Monro K, Marshall DJ: Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 2011, 65:3079-3089.
74. Arendt JD: Allocation of cells to proliferation vs. differentiation and its consequences for growth and development. J Exp Zool 2000, 288:219-234.
75. Benesh DP: Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 2011, 138:913-925.
76. Michaud M, Milinski M, Parker GA, Chubb JC: Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evol Ecol 2006, 20:39-57.
77. Dupont F, Gabrion C: The concept of specificity in the procercoid-copepod system: Bothriocephalus claviceps (Cestoda) a parasite of the eel (Anguilla anguilla). Parasitol Res 1987, 73:151-158.
78. Orr TSC, Hopkins CA: Maintenance of Schistocephalus solidus in the laboratory with observations on rate of growth of, and proglottid formation in, the plerocercoid. J Fish Res Board Can 1969, 26:741-752.
79. Van Noordwijk AJ, de Jong G: Acquisition and allocation of resources - their influence on variation in life-history tactics. Am Nat 1986, 128:137-142.
80. Reznick D, Nunney L, Tessier A: Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 2000, 15:421-425.
81. Hopkins CA: Studies on cestode metabolism. I. Glycogen metabolism in Schistocephalus solidus in vivo. J Parasitol 1950, 36:384-390.