Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-29T05:27:41.167Z Has data issue: false hasContentIssue false

Reproductive consequences of host age in a desert flea

Published online by Cambridge University Press:  20 December 2012

VICTORIA LIBERMAN
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion, Israel
IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion, Israel
A. ALLAN DEGEN
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion, Israel
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
*
*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. Tel: +972 8 6596841. Fax: +972 8 6596772. E-mail: krasnov@bgu.ac.il

Summary

We tested for the effect of age of a rodent host (Meriones crassus) on reproductive performance of fleas in terms of number and quality of offspring and predicted that fleas would perform better on juvenile and old than on subadult and adult hosts. The number of flea offspring was evaluated via egg and new imago production, while their quality was estimated via duration of development, resistance to starvation and body size. Although fleas produced more eggs when they exploited adults than when they exploited juvenile, subadult and old hosts, significantly more new imago emerged from fleas fed on juvenile and old hosts than on subadult and adult hosts. Fleas performed better when they fed on juvenile and/or old hosts than on subadult and adult hosts in 2 of 3 measures of offspring quality (duration of development and body size). Nevertheless, when offspring quality was estimated via resistance to starvation of a new imago, fleas demonstrated good performance in young (juvenile and subadult) hosts, while they performed poorly in old hosts. Thus, general reproductive performance of fleas was better when they exploited young and old hosts than when they exploited median age cohorts. However, the effect of host age on flea reproductive performance was manifested somewhat differently between (a) male and female hosts and (b) male and female flea offspring.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alarcos, A. J. and Timi, J. T. (2012). Parasite communities in three sympatric flounder species (Pleuronectiformes: Paralichthyidae). Parasitology Research 110, 21552166.CrossRefGoogle ScholarPubMed
Anand, A. N. and Lorenz, M. W. (2008). Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllus bimaculatus. Journal of Insect Physiology 54, 14041412.CrossRefGoogle ScholarPubMed
Body, G., Ferté, H., Gaillard, J.-M., Delorme, D., Klein, F. and Gilot-Fromont, E. (2011). Population density and phenotypic attributes influence the level of nematode parasitism in roe deer. Oecologia 167, 635646.CrossRefGoogle ScholarPubMed
Carlier, Y. and Truyens, C. (1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 9499.CrossRefGoogle ScholarPubMed
Clutton-Brock, T. H. and Isvaran, K. (2007). Sex differences in ageing in natural populations of vertebrates. Proceedings of the Royal Society of London, B 274, 30973104.Google Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, Il, USA.Google Scholar
Dewar, A. L., Doherty, K. V., Woods, G. M., Lyons, B. L. and Muller, H. K. (2001). Acquisition of immune function during the development of the Langerhans cell network in neonatal mice. Immunology 103, 6169.CrossRefGoogle ScholarPubMed
Fichet-Calvet, E., Wang, J., Jomaa, I., Ben Ismail, R. and Ashford, R. W. (2003). Patterns of the tapeworm Raillietina trapezoides infection in the fat sand rat Psammomys obesus in Tunisia: season, climatic conditions, host age and crowding effects. Parasitology 126, 481492.CrossRefGoogle ScholarPubMed
Fielden, L. J., Rechav, Y. and Bryson, N. R. (1992). Acquired immunity to larvae of Amblyomma marmoreum and A. hebraeum by tortoises, guinea-pigs and guinea-fowl. Medical and Veterinary Entomology 6, 251254.CrossRefGoogle Scholar
Gallie, G. J. (1973). The development of acquired resistance and age resistance to Nematodirus battus in the laboratory rabbit. Journal of Helminthology 47, 369376.CrossRefGoogle ScholarPubMed
Gilbert, L. I. and Chino, H. (1974). Transport of lipids in insects. Journal of Lipid Research 15, 439456.CrossRefGoogle ScholarPubMed
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161165.CrossRefGoogle ScholarPubMed
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. (1992). Population biology of Heligmosomoides polygyris (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749757.CrossRefGoogle Scholar
Gruver, AL., Hudson, L. L. and Sempowski, G. D. (2007). Immunosenescence of ageing. Journal of Pathology 211, 144156.CrossRefGoogle ScholarPubMed
Hasselquist, D. and Nilsson, J.-A. (2009). Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philosophical Transactions of the Royal Society, B 364, 5160.CrossRefGoogle ScholarPubMed
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London, B 276, 34773485.Google Scholar
Hinde, K. (2007). Milk composition varies in relation to the presence and abundance of Balantidium coli in the mother in captive rhesus macaques (Macaca mulatta). American Journal of Primatology 69, 625634.CrossRefGoogle Scholar
Hinkle, N. C., Koehler, P. G. and Kern, W. H. (1991). Hematophagous strategies of the cat flea (Siphonaptera: Pulicidae). Florida Entomologist 74, 377385.CrossRefGoogle Scholar
Honek, A. (1993). Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos 66, 483492.CrossRefGoogle Scholar
Hudson, P. J. and Dobson, A. P. (1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 144176. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Johansen, C. E., Lydersen, C., Aspholm, P. E., Haug, T. and Kovacs, K. M. (2010). Helminth parasites in ringed seals (Pusa hispida) from Svalbard, Norway with special emphasis on nematodes: variation with age, sex, diet, and location of host. Journal of Parasitology 96, 946953.CrossRefGoogle ScholarPubMed
Jørgensen, L. T., Leathwick, D. M., Charleston, W. A. G., Godfrey, P. L., Vlassoff, A. and Sutherland, I. A. (1998). Variation between hosts in the developmental success of the free-living stages of trichostrongyle infections of sheep. International Journal for Parasitology 28, 13471352.CrossRefGoogle ScholarPubMed
Kam, M. and Degen, A. A. (1993). Energetics of lactation and growth in the fat sand rat, Psammomys obesus. New perspectives of resource partitioning and the effect of litter lize. Journal of Theoretical Biology 162, 353369.CrossRefGoogle Scholar
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012). Feeding performance of fleas on host species: is phylogenetic distance between hosts important? Parasitology 139, 6068.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Ghazaryan, L., Krasnov, B. R. and Degen, A. A. (2008). Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent-infesting fleas. Functional Ecology 22, 530536.CrossRefGoogle Scholar
Khokhlova, I. S., Krasnov, B. R., Kam, M., Burdelova, N. I. and Degen, A. A. (2002). Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. Journal of Zoology (London) 258, 349354.CrossRefGoogle Scholar
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, 32993304CrossRefGoogle Scholar
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009). 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.CrossRefGoogle ScholarPubMed
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264.CrossRefGoogle ScholarPubMed
Knopf, P. M. and Coghlan, R. L. (1989). Maternal transfer of resistance to Schistosoma mansoni. Journal of Parasitology 75, 398404.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: a Model for Ecological Parasitology. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M. and Morand, S. (2006). Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters. Journal of Parasitology 92, 242248.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Liberman, V., Khokhlova, I. S., Degen, A. A. and Krasnov, B. R. (2011). The effect of host age on feeding performance of fleas. Parasitology 138, 11541163.CrossRefGoogle ScholarPubMed
McCoy, K. D., Boulinier, T., Schjorring, S. and Michalakis, Y. (2002). Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research 4, 441456.Google Scholar
Medvedev, S. G. and Krasnov, B. R. (2006). Fleas – permanent satellites of small mammals. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 161177. SpringerVerlag, Tokyo, Japan.CrossRefGoogle Scholar
Møller, A. P. and de Lope, F. (1999). Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. Journal of Animal Ecology 68, 163171.CrossRefGoogle Scholar
Pacala, S. W. and Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197210.CrossRefGoogle ScholarPubMed
Pelletier, F., Page, K. A., Ostiguy, T. and Festa-Bianchet, M. (2005). Fecal counts of lungworm larvae and reproductive effort in bighorn sheep, Ovis canadensis. Oikos 110, 473480.CrossRefGoogle Scholar
Praet, N., Speybroeck, N., Rodriguez-Hidalgo, R., Benitez-Ortiz, W., Berkvens, D., Brandt, J., Saegerman, C. and Dorny, P. (2010). Age-related infection and transmission patterns of human cysticercosis. International Journal for Parasitology 40, 8590.CrossRefGoogle ScholarPubMed
Rechav, Y. (1992). Naturally acquired resistance to ticks – a global view. International Journal of Tropical Insect Science 13, 495504.CrossRefGoogle Scholar
Rechav, Y., Heller-Haupt, A. and Varma, M. G. R. (1989). Resistance and cross-resistance in guinea-pigs and rabbits to immature stages of ixodid ticks. Medical and Veterinary Entomology 3, 333336.CrossRefGoogle ScholarPubMed
Rousset, F., Thomas, F., de Meeûs, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distribution of parasite loads. Ecology 77, 22032211.CrossRefGoogle Scholar
Saino, N., Calza, S. and Møller, A. P. (1997). Immunocompetence of nestling barn swallows in relation to brood size and parental effort. Journal of Animal Ecology 66, 827836.CrossRefGoogle Scholar
Saino, N., Ferrari, R. P., Romano, M., Rubolini, D. and Møller, A. P. (2003). Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica). Journal of Evolutionary Biology 16, 11271134.CrossRefGoogle ScholarPubMed
Sargison, N. D., Jackson, F. and Gilleard, J. S. (2011). Effects of age and immune suppression of sheep on fecundity, hatching and larval feeding of different strains of Haemonchus contortus. Veterinary Journal 189, 296301.CrossRefGoogle ScholarPubMed
Silverman, J. and Appel, A. G. (1994). Adult cat flea (Siphonaptera, Pulicidae) excretion of host blood proteins in relation to larval nutrition. Journal of Medical Entomology 31, 265271.CrossRefGoogle ScholarPubMed
Tarazona, R., Solana, R., Ouyang, Q. and Pawalec, G. (2002). Basic biology and clinical impact of immunosenescence. Experimental Gerontology 37, 183189.CrossRefGoogle ScholarPubMed
Tschirren, B. and Richner, H. (2006). Parasites shape the optimal investment in immunity. Proceedings of the Royal Society of London, B 273, 17731777.Google Scholar
Tripet, F., Christe, P. and Møller, A. P. (2002). The importance of host spatial distribution for parasite specialization and speciaton: a comparative study of bird fleas (Siphonaptera: Ceratophyllidae). Journal of Animal Ecology 71, 735748.CrossRefGoogle Scholar
Willadsen, P. (1980). Immunity to ticks. Advances in Parasitology 18, 293313.CrossRefGoogle ScholarPubMed
Woolhouse, M. J. E. (1998). Patterns in parasite epidemiology: the peak shift. Parasitology Today 14, 428434.CrossRefGoogle ScholarPubMed