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The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees

Published online by Cambridge University Press:  17 February 2005

A. LOGAN
Affiliation:
Department of Zoology, Trinity College Dublin, Dublin 2, Ireland
M. X. RUIZ-GONZÁLEZ
Affiliation:
Department of Zoology, Trinity College Dublin, Dublin 2, Ireland
M. J. F. BROWN
Affiliation:
Department of Zoology, Trinity College Dublin, Dublin 2, Ireland

Abstract

Host nutrition plays an important role in determining the development and success of parasitic infections. While studies of vertebrate hosts are accumulating, little is known about how host nutrition affects parasites of invertebrate hosts. Crithidia bombi is a gut trypanosome parasite of the bumble bee, Bombus terrestris and here we use it as a model system to determine the impact of host nutrition on the population dynamics and development of micro-parasites in invertebrates. Pollen-starved bees supported significantly smaller populations of the parasite. In pollen-fed bees the parasite showed a temporal pattern in development, with promastigote transmission stages appearing at the start of the infection and gradually being replaced by choanomastigote and amastigote forms. In pollen-starved bees this developmental process was disrupted, and there was no pattern in the appearance of these three forms. We discuss the implications of these results for parasite transmission, and speculate about the mechanisms behind these changes.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ANSTEAD, G. M., CHANDRASEKAR, B., ZHAO, W. G., YANG, J., PEREZ, L. E. & MELBY, P. C. ( 2001). Malnutrition alters the innate immune response and increases early visceralization following Leishmania donovani infection. Infection and Immunity 69, 47094718.CrossRefGoogle Scholar
BROWN, M. J. F., LOOSLI, R. & SCHMID-HEMPEL, P. ( 2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421427.CrossRefGoogle Scholar
BROWN, M. J. F., MORET, Y. & SCHMID-HEMPEL, P. ( 2003). Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parasitology 126, 253260.CrossRefGoogle Scholar
BROWN, M. J. F., SCHMID-HEMPEL, R. & SCHMID-HEMPEL, P. ( 2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72, 9941002.CrossRefGoogle Scholar
BUNDY, D. A. P. & GOLDEN, M. H. N. ( 1987). The impact of host nutrition on gastro-intestinal helminth populations. Parasitology 95, 623635.CrossRefGoogle Scholar
COOP, R. L. & KYRIAZAKIS, I. ( 2001). Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325330.CrossRefGoogle Scholar
DURRER, S. & SCHMID-HEMPEL, P. ( 1994). Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London, B 258, 299302.CrossRefGoogle Scholar
EZENWA, V. O. ( 2004). Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology 34, 535542.CrossRefGoogle Scholar
HOCHBERG, Y. ( 1988). A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800802.CrossRefGoogle Scholar
HOLMES, P. H., KATUNGUKA-RWAKISHAYA, E., BENNISON, J. J., WASSINK, G. J. & PARKINS, J. J. ( 2000). Impact of nutrition on the pathophysiology of bovine trypanosomiasis. Parasitology 120, S73S85.CrossRefGoogle Scholar
IMHOOF, B. & SCHMID-HEMPEL, P. ( 1998). Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331336.CrossRefGoogle Scholar
IMHOOF, B. & SCHMID-HEMPEL, P. ( 1999). Colony success of Bombus terrestris and microparasitic infections in the field. Insectes Sociaux 46, 223238.Google Scholar
ING, R., SU, Z., SCOTT, M. E. & KOSKI, K. G. ( 2000). Suppressed T helper 2 immunity and prolonged survival of a nematode parasite in protein-malnourished mice. Proceedings of the National Academy of Sciences, USA 97, 70787083.CrossRefGoogle Scholar
KEYMER, A., CROMPTON, D. W. T. & WALTERS, D. E. ( 1983). Parasite population biology and host nutrition – dietary fructose and moniliformis (Acanthocephala). Parasitology 87, 265278.CrossRefGoogle Scholar
KOLLIEN, A. H. & SCHAUB, G. A. ( 2000). The development of Trypanosoma cruzi in Triatominae. Parasitology Today 16, 381387.CrossRefGoogle Scholar
KOLLIEN, A. H. & SCHAUB, G. A. ( 2002). The development of Blastocrithidia triatomae (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of starvation. Parasitology Research 88, 804809.CrossRefGoogle Scholar
KOLLIEN, A. H. & SCHAUB, G. A. ( 2003). The development of Blastocrithidia triatomae (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of feeding. Parasitology Research 89, 430436.Google Scholar
KOSKI, K. G. & SCOTT, M. E. ( 2001). Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition 21, 297321.CrossRefGoogle Scholar
MORET, Y. & SCHMID-HEMPEL, P. ( 2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 11661168.CrossRefGoogle Scholar
NEVES, R. H., MACHADO-SILVA, J. R., PELAJO-MACHADO, M., OLIVEIRA, S. A., COUTINHO, E. M., LENZI, H. L. & GOMES, D. C. ( 2001). Morphological aspects of Schistosoma mansoni adult worms isolated from nourished and undernourished mice: a comparative analysis by confocal laser scanning microscopy. Memorias do Instituto Oswaldo Cruz 96, 10131016.CrossRefGoogle Scholar
OLIVEIRA, S. A., BARBOSA, A. A., GOMES, D. C., MACHADO-SILVA, J. R., BARROS, A. F., NEVES, R. H. & COUTINHO, E. M. ( 2003). Morphometric study of Schistosoma mansoni adult worms recovered from undernourished infected mice. Memorias do Instituto Oswaldo Cruz 98, 623627.CrossRefGoogle Scholar
ONGELE, E. A., ASHRAF, M., NESBITT, R. A., HUMPHREY, P. A. & LEE, C. M. ( 2002). Effects of selenium deficiency in the development of trypanosomes and humoral immune responses in mice infected with Trypanosoma musculi. Parasitology Research 88, 540545.CrossRefGoogle Scholar
PEDERSEN, S., SAEED, I., MICHAELSEN, K. F., FRIIS, H. & MURRELL, K. D. ( 2002). Impact of protein energy malnutrition on Trichuris suis infection in pigs concomitantly infected with Ascaris suum. Parasitology 124, 561568.CrossRefGoogle Scholar
PETKEVICIUS, S., KNUDSEN, K. E. B., NANSEN, P. & MURRELL, K. D. ( 2001). The effect of dietary carbohydrates with different digestibility on the populations of Oesophagostomum dentatum in the intestinal tract of pigs. Parasitology 123, 315324.CrossRefGoogle Scholar
SCHMID-HEMPEL, P. ( 2001). On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88, 147158.CrossRefGoogle Scholar
SCHMID-HEMPEL, P., PUHR, K., KRUGER, N., REBER, C. & SCHMID-HEMPEL, R. ( 1999). Dynamic and genetic consequences of variation in horizontal transmission for microparasitic infection. Evolution 53, 426434.CrossRefGoogle Scholar
SCHMID-HEMPEL, P. & SCHMID-HEMPEL, R. ( 1993). Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behavioral Ecology and Sociobiology 33, 319327.CrossRefGoogle Scholar
SCOTT, M. E. & KOSKI, K. G. ( 2000). Zinc deficiency impairs immune responses against parasitic nematode infections at intestinal and systemic sites. Journal of Nutrition 130, 1412S1420S.CrossRefGoogle Scholar
SHI, H. N., SCOTT, M. E., KOSKI, K. G., BOULAY, M. & STEVENSON, M. M. ( 1995). Energy restriction and severe zinc-deficiency influence growth, survival and reproduction of Heligmosomoides polygyrus (Nematoda) during primary and challenge infections in mice. Parasitology 110, 599609.CrossRefGoogle Scholar
SHI, H. N., SCOTT, M. E., STEVENSON, M. M. & KOSKI, K. G. ( 1994). Zinc-deficiency impairs T-cell function in mice with primary infection of Heligmosomoides polygyrus (Nematoda). Parasite Immunology 16, 339350.CrossRefGoogle Scholar
SHYKOFF, J. A. & SCHMID-HEMPEL, P. ( 1991 a). Parasites and the advantage of genetic variability within social insect colonies. Proceedings of the Royal Society of London, B 243, 5558.Google Scholar
SHYKOFF, J. A. & SCHMID-HEMPEL, P. ( 1991 b). Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups. Behavioral Ecology and Sociobiology 28, 371376.Google Scholar
SHYKOFF, J. A. & SCHMID-HEMPEL, P. ( 1991 c). Incidence and effects of four parasites in natural populations in bumble bees in Switzerland. Apidologie 22, 117126.Google Scholar
SHYKOFF, J. A. & SCHMID-HEMPEL, P. ( 1991 d). Parasites delay worker reproduction in bumblebees: consequences for eusociality. Behavioral Ecology 2, 242248.Google Scholar
SIMOES, C., NEVES, R. H., BARROS, L. D., BRITO, P. D., CRAVO, C. O., DE MOURA, E. G. & MACHADO-SILVA, J. R. ( 2002). Parasitological characteristics of Schistosoma mansoni infection in Swiss mice with underlying malnutrtion. Memorias do Instituto Oswaldo Cruz 97, 143147.CrossRefGoogle Scholar
SMEETS, P. & DUCHATEAU, M. J. ( 2003). Longevity of Bombus terrestris workers (Hymenoptera: Apidae) in relation to pollen availability, in the absence of foraging. Apidologie 34, 333337.CrossRefGoogle Scholar
SUDATI, J. E., RIVAS, F. & FRIED, B. ( 1997). Effect of a high protein diet on worm recovery, growth and distribution of Echinostoma caproni in ICR mice. Journal of Helminthology 71, 351354.CrossRefGoogle Scholar