Skip to main content Accessibility help
×
Home

Host reproductive status and reproductive performance of a parasite: offspring quality and trade-offs in a flea parasitic on a rodent

  • ELIZABETH M. DLUGOSZ (a1), CYNTHIA J. DOWNS (a2), IRINA S. KHOKHLOVA (a3), A. ALLAN DEGEN (a3) and BORIS R. KRASNOV (a1)...

Summary

We investigated offspring quality in fleas (Xenopsylla ramesis) feeding on non-reproducing, pregnant or lactating rodents (Meriones crassus) and asked whether (a) quality of flea offspring differs dependent on host reproductive status; (b) fleas trade off offspring quantity for quality; and (c) quality variables are inter-correlated. Emergence success was highest when parents exploited pregnant hosts, while development time was longest when parents exploited lactating hosts. Male offspring from fleas fed on non-reproductive and pregnant hosts were larger than those from lactating hosts whereas female offspring from fleas fed on pregnant hosts were larger than those from both lactating and non-reproductive hosts. Male offspring survived under starvation the longest when their parents exploited lactating hosts and the shortest when their parents exploited pregnant hosts. Female offspring of parents that exploited lactating hosts survived under starvation longer than those that exploited non-reproductive and pregnant hosts. Emergence success and development time decreased as mean number of eggs laid by mothers increased. Fleas that were larger and took longer to develop lived significantly longer under starvation. These results indicate the presence of a trade-off between offspring quantity and quality in fleas exploiting female Sundevall's jird in varying reproductive condition but this trade-off depended on the quality trait considered.

Copyright

Corresponding author

* Corresponding author: Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. E-mail: krasnov@bgu.ac.il

References

Hide All
Arrese, E. L. and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207225.
Burton-Chellew, M. N., Sykes, E. M., Patterson, S., Shuker, D. M. and West, S. A. (2007). The cost of mating and the relationship between body size and fitness in males of the parasitoid wasp Nasonia vitripennis . Evolutionary Ecology Research 9, 921934.
Campbell, B. C. and Duffey, S. S. (1979). Effect of density and instar of Heliothis zea on parasitization by Hyposoter exiguae . Environmental Entomology 8, 127130.
Davidowitz, G., D'Amico, L. J. and Nijhout, H. F. (2003). Critical weight in the development of insect body size. Evolution and Development 5, 188197.
Degen, A. A. (1997). Ecophysiology of Small Desert Mammals. Springer, Berlin, Germany.
Degen, A. A., Khokhlova, I. S. and Kam, M. (2011). Milk production of the dam limits the growth rate of Sundevall's jird (Meriones crassus) pups. Mammalian Biology 76, 285289.
Dlugosz, E. M., Downs, C. J., Khokhlova, I. S., Degen, A. A. and Krasnov, B. R. (2014). Ectoparasite performance when feeding on reproducing mammalian females: an unexpected decrease when on pregnant hosts. Journal of Experimental Biology (in press).
Esperk, T. and Tammaru, T. (2010). Size compensation in moth larvae: attention to larval instars. Physiological Entomology 35, 222230.
Fischer, B., Taborsky, B. and Kokko, H. (2011). How to balance the offspring quality-quantity trade-off when environmental cues are unreliable. Oikos 120, 258270.
Fox, C. W. and Czesak, M. E. (2000). Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45, 341369.
Ghimire, M. N. and Phillips, T. W. (2010). Suitability of different lepidopteran host species for development of Bracon hebetor (Hymenoptera: Braconidae). Environmental Entomology 39, 449458.
Giron, D. and Casas, J. (2003). Mothers reduce egg provisioning with age. Ecology Letters 6, 273277.
Hanks, L. M., Millar, J. G. and Paine, T. D. (1996). Body size influences mating success of the Eucalyptus longhorned borer (Coleoptera: Cerambycidae). Journal of Insect Behavior 9, 369382.
Honek, A. (1993). Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66, 483492.
Hothorn, T., Bretz, F. and Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.
Kam, M., Cohen-Gross, S., Khokhlova, I. S., Degen, A. A. and Geffen, E. (2003). Average daily metabolic rate, reproduction and energy allocation during lactation in the Sundevall Jird Meriones crassus . Functional Ecology 17, 496503.
Khokhlova, I. S., Kam, M., Gonen, S. and Degen, A. A. (2000). Level of energy intake affects the estrous cycle in Sundevall's jird (Meriones crassus). Physiological and Biochemical Zoology 73, 257263.
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 a). Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus? Journal of Experimental Biology 212, 14291435.
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 b). Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitology Research 105, 16671673.
Khokhlova, I. S., Serobyan, V., Degen, A. A. and Krasnov, B. R. (2010). Host gender and offspring quality in a flea parasitic on a rodent. Journal of Experimental Biology 213, 32993304.
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012). Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. Journal of Evolutionary Biology 25, 20052013.
Khokhlova, I. S., Pilosof, S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2014). A trade-off between quantity and quality of offspring in haematophagous ectoparasites: the effect of the level of specialization. Journal of Animal Ecology (in press).
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S., Degen, A. A. and Rogovin, K. V. (1996). On the biology of Sundevall's jird (Meriones crassus Sundevall) in Negev Highlands, Israel. Mammalia 60, 375391.
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001). Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Medical and Veterinary Entomology 15, 249258.
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002). Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 7081.
Krasnov, B. R., Burdelov, S. A., Khokhlova, I. S. and Burdelova, N. V. (2003). Sexual size dimorphism, morphological traits and jump performance in seven species of desert fleas (Siphonaptera). Journal of Zoology (London) 261, 181189.
Krasnov, B. R., Burdelova, N. V., Khokhlova, I. S., Shenbrot, G. I. and Degen, A. A. (2005). Larval interspecific competition in two flea species parasitic on the same rodent host. Ecological Entomology 30, 146155.
Lack, D. (1947). The significance of clutch-size. Ibis 89, 302352.
Lawrence, W. and Foil, L. D. (2002). The effects of diet upon pupal development and cocoon formation by the cat flea (Siphonaptera: Pulicidae). Journal of Vector Ecology 27, 3943.
Liberman, V., Khokhlova, I. S., Degen, A. A. and Krasnov, B. R. (2013). Reproductive consequences of host age in a desert flea. Parasitology 140, 461470.
Luong, L. T., Grear, D. A. and Hudson, P. J. (2009). Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. International Journal for Parasitology 39, 12631268.
Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends in Ecology and Evolution 16, 254260.
Nijhout, H. F. (1979). Stretch-induced moulting in Oncopeltus fasciatus . Journal of Insect Physiology 25, 277281.
Nijhout, H. F. (1994). Insect Hormones. Princeton University Press, Princeton, NJ, USA.
Nijhout, H. F. (2003). The control of body size in insects. Developmental Biology 261, 19.
Nijhout, H. F., Davidowitz, G. and Roff, D. A. (2006). A quantitative analysis of the mechanism that controls body size in Manduca sexta . Journal of Biology 5, article 16. doi: 10.1186/jbiol43.
Parker, G. A. and Begon, M. (1986). Optimal egg size and clutch size – effects of environment and maternal phenotype. American Naturalist 128, 573592.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and the R Development Core Team (2013). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-108.
R Development Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/.
Riquelme, C., George-Nascimento, M. and Balboa, L. (2006). Morphometry and fecundity of Profilicollis bullocki Mateo, Córdova & Guzmán 1982 (Acanthocephala: Polymorphidae) in sympatric coastal bird species of Chile. Revista Chilena de Historia Natural 79, 465474.
Schmid-Hempel, R. and Schmid-Hempel, P. (1996). Host choice and fitness correlates for conopid flies parasitising bumblebees. Oecologia 107, 7178.
Smith, C. C. and Fretwell, S. D. (1974). Optimal balance between size and number of offspring. American Naturalist 108, 499506.
Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society of London B 363, 375398.
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford University Press, New York, NY, USA.
Taborsky, B. (2006). The influence of juvenile and adult environments on life-history trajectories. Proceedings of the Royal Society of London B 273, 741750.
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Functional Ecology 21, 372378.
Veena, M. and Manjunath, D. (2013). Does host age affect progeny production and progeny fitness in Trichopria sp.? BioControl 58, 299307.
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, 393425.
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY, USA.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed