Oecologia

, Volume 134, Issue 4, pp 479–486 | Cite as

Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails

Population Ecology
First Online:
Received:
Accepted:

Abstract

Resource allocation strategies may be influenced by both biotic and abiotic factors. The purpose of this study was to investigate the effects of both parasitism and diet quality on the growth, reproduction, and survival of the pond snail, Lymnaea elodes. In addition, we assessed parasite growth and reproduction. High-protein (high diet) or low-protein diets (low diet) were fed to juvenile L. elodes snails that were either exposed or sham-exposed to the castrating trematode, Echinostoma revolutum. Host growth was assessed weekly; reproduction and survival were recorded every 2–3 days. We estimated parasite development as the time to parasite release from the host (patency), and parasite reproduction as the number of larvae shed from infected snails at two time points. Diet and infection status had significant effects on snail growth. Infected snails produced few eggs and tended to grow to larger sizes than uninfected snails regardless of diet. In contrast, exposed-uninfected individuals displayed diet-dependent patterns of growth and reproduction. On the high-protein diet, uninfected and exposed-uninfected snails exhibited similar patterns of growth and reproduction, whereas in the low-diet treatment, exposed-uninfected snails exhibited reduced growth and delayed reproduction relative to uninfected individuals. Survival differed among treatments in the latter stages of the study with infected snails exhibiting reduced survival relative to snails from other treatments. Moreover, infected low-diet snails exhibited lower survival than infected high-diet snails. Parasite development and reproduction did not appear to be directly influenced by the quality of host diet. Results from this study suggest that energy allocation patterns are context-dependent in juvenile snails, influenced by parasite exposure and diet quality. Furthermore, parasite reproduction appears to depend more on host size than on the quality of host diet.

Keywords

Resource allocation Trade-offs Host diet Lymnaea Echinostoma 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We wish to thank R. Howard, J. Jokkela, M. Levy, R. Sorensen, E. Wetzel, and an anonymous reviewer for constructive comments on the manuscript. We would also like to acknowledge N. Carmosini for her help collecting and maintaining snails. This research was supported by grants from NSERC Canada and the Indiana Academy of Science to G. S.

References

  1. Bourns TK (1974) Carbohydrate and protein in Lymnaea stagnalis eggs and Trichobilharzia ocellata cercariae. J Parasitol 60:1046–1047PubMedGoogle Scholar
  2. Brown KM (1982) Resource overlap and competition in pond snails: an experimental analysis. Ecology 63:412–422Google Scholar
  3. Brown KM, Leathers BK, Minchella DJ (1988) Trematode prevalence and the population dynamics of freshwater pond snails. Am Midl Nat 120:289–301Google Scholar
  4. Chase JM (1999) To grow or to reproduce? The role of life-history plasticity in food web dynamics. Am Nat 154:571–586CrossRefPubMedGoogle Scholar
  5. Coop RL, Holmes PH (1996) Nutrition and parasite interactions. Int J Parasitol 26:951–962CrossRefPubMedGoogle Scholar
  6. Crompton DWT (1987) Host diet as a determinant of parasite growth, reproduction and survival. Mammal Rev 17:117–126Google Scholar
  7. Daras MR, Sisbarro S, Fried B (2000) Effects of a high-carbohydrate diet on growth of Echinostoma caproni in ICR mice. Comp Parasitol 67:241–243Google Scholar
  8. Dikkeboom R, Van der Knapp WPW, Meuleman EA, Sminia T (1984) Differences between blood cells of juvenile and adult specimens of the pond snails Lymnaea stagnalis. Cell Tissue Res 238:43–47Google Scholar
  9. Doughty P, Shine R (1998) Reproductive energy allocation and long-term energy stores in a viviparous lizard (Eulamprus tympanum). Ecology 79:1073–1083Google Scholar
  10. Doums C, Perdieu M, Jarne P (1998) Resource allocation and stressful conditions in the aphallic snail Bulinus truncatus. Ecology 79:720–733Google Scholar
  11. Fernandez JC, Esch GW (1991) Effects of parasitism on the growth rate of the pulmonate snail Helisoma anceps. J Parasitol 77:540–550PubMedGoogle Scholar
  12. Fried B, Muller EE, Broadway J, Sherma J (2001) Effects of diet on the development of Schistosoma mansoni in Biomphalaria glabrata and on the neutral lipid content of the digestive gland-gonad complex of the snail. J Parasitol 87:223–225CrossRefPubMedGoogle Scholar
  13. Gerard C, Theron A (1997) Age/size- and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata. Oecologia 112:447–452CrossRefGoogle Scholar
  14. Hoang A (2001) Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55:2353–2358PubMedGoogle Scholar
  15. Hodasi JKM (1972) The effects of Fasciola hepatica on Lymnaea trunculata. Parasitology 65:359–369PubMedGoogle Scholar
  16. Huffman JE, Fried B (1990) Echinostoma and echinostomiasis. Adv Parasitol 29:215–269PubMedGoogle Scholar
  17. Jokela J, Uotila L, Taskinen J (1993) Effects of the castrating trematode parasite Rhipidocotyle fennica on energy allocation of the freshwater clam Anodonta piscinalis. Funct Ecol 7:332–338Google Scholar
  18. Jokela J, Lively CM, Taskinen J, Peters AD (1999) Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum). Oecologia 119:320–325.CrossRefGoogle Scholar
  19. Keas BE, Esch GW (1997) The effects of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis. J Parasitol 83:96–104PubMedGoogle Scholar
  20. Kendall SB (1949) Nutritional factors affecting the rate of development of Fasciola hepatica in Limnaea trunculata. J Helminthol 23:179–190Google Scholar
  21. Kern S, Ackermann M, Stearns SC, Kawecki TJ (2001) Decline in offspring viability as a manifestation of aging in Drosophila melanogaster. Evolution 55:1822–1831PubMedGoogle Scholar
  22. Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280PubMedGoogle Scholar
  23. Kuris AM (1980) Effect of exposure to Echinostoma liei on growth and survival of young Biomphalaria glabrata snails. Int J Parasitol 10:303–308CrossRefPubMedGoogle Scholar
  24. Kuris AM, Warren J (1980) Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second intermediate host, Biomphalaria glabrata. J Parasitol 66:630–635PubMedGoogle Scholar
  25. Langand J, Jourdane J, Coustau C, Delay B, Morand S (1998) Cost of resistance, expressed as a delayed maturity, detected in the host-parasite system Biomphalaria glabrata/Echinostoma caproni. Heredity 80:320–325CrossRefGoogle Scholar
  26. Loker ES (1979) Effects of Schistosomatium douthetti infection on the growth, survival and reproduction of Lymnaea catascopium. J Invert Pathol 34:138–144Google Scholar
  27. Loker ES, Adema CM (1995) Schistosomes, echinostomes and snails:comparative immunobiology. Parasitol Today 11:120–124CrossRefGoogle Scholar
  28. Makanga B (1981) The effect of varying the number of Schistosoma mansoni miracidia on the reproduction and survival of Biomphalaria pfeifferi. J Invert Pathol 37:7–10Google Scholar
  29. McClelland G, Bourns TKR (1969) Effects of Trichobilharzia ocellata on growth, reproduction and survival of Lymnaea stagnalis. Exp Parasitol 24:137–146PubMedGoogle Scholar
  30. Minchella DJ (1985) Host life history variation in response to parasitism. Parasitology 90:205–216Google Scholar
  31. Minchella DJ, Loverde PT (1981) A cost of early reproductive effort in the snail, Biomphalaria glabrata. Am Nat 118:876–881CrossRefGoogle Scholar
  32. Moller AP (1995) Hormones, handicaps and bright birds. Trends Ecol Evol 10:121–121CrossRefGoogle Scholar
  33. Moret Y, Schmidt-Hempel P ( 2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1198PubMedGoogle Scholar
  34. Probst S, Kube J (1999) Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia vetrosa (Gastropoda:Prosobranchia)? J Exp Mar Biol 238:49–68CrossRefGoogle Scholar
  35. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267Google Scholar
  36. Rigby MC, Jokela J (2000) Predator avoidance and immune defence:costs and trade-offs in snails. Proc R Soc Lond 267:171–176CrossRefGoogle Scholar
  37. Rigby MC, Hechinger RF, Stevens L (2002) Why should resistance be costly? Trends Parasitol 18:116–120CrossRefPubMedGoogle Scholar
  38. Roff DA (1992) The evolution of life histories:theory and analysis. Chapman and Hall, New YorkGoogle Scholar
  39. Rollo CD, Hawryluk MD (1988) Compensatory scope and resource allocation in two species of aquatic snails. Ecology 69:146–156Google Scholar
  40. Rosario C, Fried B (1999) Effects of a protein-free diet on worm recovery, growth, and distribution of Echinostoma caproni in ICR mice. J Helminthol 73:167–169PubMedGoogle Scholar
  41. Saino N, Moller AP (1996) Sexual ornamentation and immunocompetence in the barn swallow. Behav Ecol 7:227–232Google Scholar
  42. Sandland GJ, Goater CP (2001) Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows. J Parasitol 87:267–272PubMedGoogle Scholar
  43. Sapp KK, Loker ES (2000) Mechanisms underlying digenean-snail specificity: role of miracidial attachment and host plasma factors. J Parasitol 86:1012–1019PubMedGoogle Scholar
  44. Schawang JE, Janovy J (2001) The response of Gregarina niphandrodes (Apicomplexa: Eugregarinida: Septatina) to host starvation in Tenebrio molitor (Coleoptera: Tenebrionidae) adults. J Parasitol 87:600–605PubMedGoogle Scholar
  45. Sorensen RE, Minchella DJ (1998) Parasite influences on host life history: Echinostoma revolutum parasitism in Lymnaea elodes snails. Oecologia 115:188–195CrossRefGoogle Scholar
  46. Sorensen RE, Minchella DJ (2001) Snail-trematode life-history interactions: past trends and future directions. Parasitology 123:S1-S16CrossRefGoogle Scholar
  47. Stearns SC (1993) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  48. Thompson S, Mejiascales V, Borchardt D (1991) Physiological-studies of snail-schistosome interactions and potential for improvement of in vitro culture of schistosomes. In Vitro Cell Dev B 27:497–504.Google Scholar
  49. Van der Knapp W, Adema C, Sminia T (1993) Invertebrate blood cells:morphological and functional aspects of the haemocytes of the pond snail Lymnaea stagnalis. Comp Haematol Int 3:20–26Google Scholar
  50. Weimerskirch H, Cherel Y, Cuenot Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female wandering albatrosses Ecology 78:2051–2063Google Scholar
  51. Zakikhani M, Rau ME (1999) Plagiorchis elegans (Digenea: Plagiorchidae) infections in Stagnicola elodes (Pulmonata: Lymnaeidae): host susceptibility, growth, reproduction, mortality and cercarial production. J Parasitol 85:454–463PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Biological SciencesPurdue UniversityWest LafayetteUSA

Personalised recommendations