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Energy expenditure for egg production in arthropod ectoparasites: the effect of host species

Published online by Cambridge University Press:  10 May 2013

IRINA S. KHOKHLOVA ,
LAURA J. FIELDEN ,
JOSEPH B. WILLIAMS ,
A. ALLAN DEGEN  and
BORIS R. KRASNOV
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, Midreshet Ben-Gurion, Israel
LAURA J. FIELDEN
Affiliation:
School of Science and Math, Truman State University, Kirksville, MO, USA
JOSEPH B. WILLIAMS
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH, USA
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, 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, 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. E-mail: [email protected]
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Summary

We studied the energy cost of egg production in two flea species (Parapulex chephrenis and Xenopsylla ramesis) feeding on principal (Acomys cahirinus and Meriones crassus, respectively) and auxiliary (M. crassus and A. cahirinus, respectively) rodent hosts. We predicted that fleas feeding on principal as compared with auxiliary hosts will (a) expend less energy for egg production; (b) produce larger eggs and (c) live longer after oviposition. Both fleas produced more eggs and spent less energy per egg when exploiting principal hosts. Parapulex chephrenis produced larger eggs after exploiting auxiliary hosts, while the opposite was true for X. ramesis. After oviposition, P. chephrenis fed on the auxiliary hosts survived for a shorter time than those fed on the principal hosts, while in X. ramesis the survival time did not differ among hosts. Our results suggested that one of the proximate causes for lower reproductive performance and subsequent lower abundance of fleas on auxiliary hosts is the higher energy cost of egg production. However, in some species, lower offspring number may be compensated to some extent by their size, although this compensation may also compromise their future reproduction via decreased survival. In addition, the reproductive strategy of exploitation of low profitable (i.e. auxiliary) hosts may differ between flea species.

Keywords

Bloodegg productionenergyfleashosts
Type
Research Article
Information
Parasitology , Volume 140 , Issue 9 , August 2013 , pp. 1070 - 1077
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Arbiv, A., Khokhlova, I. S., Ovadia, O., Novoplansky, A. and Krasnov, B. R. (2012). Use it or lose it: reproductive implications of experimental host shifting in a haematophagous ectoparasite. Journal of Evolutionary Biology 25, 1140–1147.CrossRefGoogle Scholar
Arrese, E. L. and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–225.CrossRefGoogle ScholarPubMed
Bell, G. and Koufopanou, V. (1986). The cost of reproduction. Oxford Surveys in Evolutionary Biology 3, 83–131.Google Scholar
Brooks, D. R., León-Règagnon, V., McLennan, D. A. and Zelmer, D. (2006). Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, S76–S85.CrossRefGoogle ScholarPubMed
Canavoso, L. E., Jouni, Z. E., Karnas, K. J., Pennington, J. E. and Wells, M. A. (2001). Fat metabolism in insects. Annual Review of Nutrition 21, 23–46.CrossRefGoogle ScholarPubMed
Carriere, Y. and Roff, D. A. (1995). The evolution of offspring size and number: a test of the Smith–Fretwell model in three species of crickets. Oecologia 102, 389–396.CrossRefGoogle ScholarPubMed
Charnov, E. L. (1993). Life History Invariants. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Choshniak, Y. and Yahav, S. (1987). Can desert rodents better utilize low quality roughage than their non-desert kindred? Journal of Arid Environments 12, 241–246.CrossRefGoogle Scholar
Cox, R. M., Parker, E. U., Cheney, D. M., Liebl, A. L., Martin, L. B. and Calsbeek, R. (2010). Experimental evidence for physiological costs underlying the trade-off between reproduction and survival. Functional Ecology 24, 1262–1269.CrossRefGoogle Scholar
Czesak, M. E. and Fox, C. W. (2003). Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments. Evolution 57, 1121–1132.Google Scholar
Dean, R. L., Collins, J. V. and Locke, M. (1985). Structure of the fat body. In Comprehensive Insect Physiology, Biochemistry, and Pharmacology (ed. Kerkut, G. A. and Gilbert, L. I.), pp. 155–210. Pergamon Press, New York, USA.Google Scholar
Degen, A. A. (1997). Ecophysiology of Small Desert Mammals. SpringerVerlag, Berlin, Germany.CrossRefGoogle Scholar
Doughty, P. and Shine, R. (1997). Detecting life history trade-offs: measuring energy stores in ‘capital’ breeders reveals costs of reproduction. Oecologia 110, 508–513.CrossRefGoogle ScholarPubMed
Fielden, L. J., Krasnov, B. R., Khokhlova, I. S. and Arakelyan, M. S. (2004). Respiratory gas exchange in the desert flea Xenopsylla ramesis (Siphonaptera: Pulicidae): response to temperature and blood-feeding. Comparative Biochemistry and Physiology A 137, 557–565.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Clarendon Press, Oxford, UK.CrossRefGoogle Scholar
Ghalambor, C. K. and Martin, T. E. (2001). Fecundity-survival trade-offs and parental risk-taking in birds. Science 292, 494–497.CrossRefGoogle ScholarPubMed
Janzen, D. H. (1985). On ecological fitting. Oikos 45, 308–310.CrossRefGoogle Scholar
Johnston, M., Johnston, D. and Richardson, A. (2005). Digestive capabilities reflect the major food sources in three species of talitrid amphipods. Comparative Biochemistry and Physiology B 140, 251–257.CrossRefGoogle ScholarPubMed
Harrington, L. C., Edman, J. D. and Scott, T. W. (2001). Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? Journal of Medical Entomology 38, 411–422.CrossRefGoogle ScholarPubMed
Harvey, G. T. (1983 a). A geographical cline in egg weights in Choristoneura fumiferana (Lepidoptera: Tortricidae) and its significance in population dynamics. Canadian Entomologist 115, 1103–1108.CrossRefGoogle Scholar
Harvey, G. T. (1983 b). Environmental and genetic effects on mean egg weight in spruce budworm (Lepidoptera: Tortricidae). Canadian Entomologist 115, 1109–1117.CrossRefGoogle Scholar
Kam, M., Khokhlova, I. S. and Degen, A. A. (1997). Granivory and plant selection by desert gerbils of different body size. Ecology 78, 2218–2229.CrossRefGoogle Scholar
Karlsson, B. (1987). Variation in egg weight, oviposition rate and reproductive reserves with female age in a natural population of the speckled wood butterfly, Pararge aegeria. Ecological Entomology 12, 473–476.CrossRefGoogle Scholar
Kearny, M. (2012). Metabolic theory, life history and the distribution of a terrestrial ectotherm. Functional Ecology 26, 167–179.CrossRefGoogle Scholar
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 a). Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitology Research 105, 1667–1673.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 b). 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, 1429–1435.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Degen, A. A. and Krasnov, B. R. (2010 a). Host gender and offspring quality in a flea parasitic on a rodent. Journal of Experimental Biology 213, 3299–3304.CrossRefGoogle Scholar
Khokhlova, I. S., Hovhanyan, A., Degen, A. A. and Krasnov, B. R. (2010 b). The effect of larval density on pre-imaginal development in two species of desert fleas. Parasitology 137, 1925–1935.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012 a). Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. Journal of Evolutionary Biology 25, 2005–2013.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012 b). Digesting blood of an auxiliary host in fleas: effect of phylogenetic distance from a principal host. Journal of Experimental Biology 215, 1259–1265.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., Shenbrot, G. I., Medvedev, S. G., Vashchenok, V. S. and Khokhlova, I. S. (1997). Host–habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159–173.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Hastriter, M., Medvedev, S. G., Shenbrot, G. I., Khokhlova, I. S. and Vashchenok, V. S. (1999). Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel Journal of Zoology 45, 333–340.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001). The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629–637.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Oguzoglu, I. and Burdelova, N. V. (2002). Host discrimination by two desert fleas using an odour cue. Animal Behaviour 64, 33–40.CrossRefGoogle Scholar
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V. and Degen, A. A. (2003). Host-specificity and foraging efficiency in blood-sucking parasites: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitology Research 90, 393–399.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Burdelov, S. A. and Fielden, L. J. (2004 a). Metabolic rate and jumping performance in seven species of desert fleas. Journal of Insect Physiology 50, 149–156.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. (2004 b). Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals. International Journal for Parasitology 34, 1289–1297.CrossRefGoogle ScholarPubMed
Lee, J. C. and Heimpel, G. E. (2008). Floral resources impact longevity and oviposition rate of a parasitoid in the field. Journal of Animal Ecology 77, 565–572.CrossRefGoogle ScholarPubMed
Lee, W. B. and Houston, D. C. (1993). The effect of diet quality on gut anatomy in British voles (Microtinae). Journal of Comparative Physiology B 163, 337–339.CrossRefGoogle ScholarPubMed
Lighton, J. R. B., Fielden, L. J. and Rechav, Y. (1993). Discontinuous ventilation in a non-insect, the tick Amblyomma marmoreum (Acari, Ixodidae): characterization and metabolic modulation. Journal of Experimental Biology 180, 229–245.CrossRefGoogle Scholar
Morrongiello, J. R., Bond, N. R., Crook, D. A. and Wong, B. B. (2012). Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish. Journal of Animal Ecology 81, 806–817.CrossRefGoogle Scholar
Murphy, D. D., Launer, A. E. and Ehrlich, P. R. (1983). The role of adult feeding in egg production and population dynamics of the checkerspot butterfly Euphydryas editha. Oecologia 56, 257–263.CrossRefGoogle ScholarPubMed
Nuismer, S. L. and Thompson, J. N. (2006). Coevolutionary alternation in antagonistic interactions. Evolution 60, 2207–2217.CrossRefGoogle ScholarPubMed
Orrell, K. S., Congdon, J. D., Jenssen, T. A., Michener, R. H. and Kunz, T. H. (2004). Intersexual differences in energy expenditure of Anolis carolinensis lizards during breeding and postbreeding seasons. Physiological and Biochemical Zoology 77, 50–64.CrossRefGoogle ScholarPubMed
Park, J. H., Attardo, G. M., Hansen, I. A. and Raikhel, A. S. (2006). GATA factor translation is the final downstream step in the amino acid/target-of-rapamycin-mediated vitellogenin gene expression in the anautogenous mosquito Aedes aegypti. Journal of Biological Chemistry 281, 11167–11176.CrossRefGoogle ScholarPubMed
Parker, G. A. and Begon, M. (1986). Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist 128, 573–592.CrossRefGoogle Scholar
Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution 18, 228–233.CrossRefGoogle Scholar
Pöykkö, H. and Mänttäri, S. (2012). Egg size and composition in an ageing capital breeder – consequences for offspring performance. Ecological Entomology 37, 330–341.CrossRefGoogle Scholar
Ricklefs, R. E. and Wikelski, M. (2002). The physiology-life history nexus. Trends in Ecology and Evolution 17, 462–468.CrossRefGoogle Scholar
Ruohomäki, K., Hanhimäki, S. and Haukioja, E. (1993). Effects of egg size, laying order and larval density on performance of Epirrita autumnata (Lep., Geometridae). Oikos 68, 61–66.CrossRefGoogle Scholar
Sarfati, M., Krasnov, B. R., Ghazaryan, L., Khokhlova, I. S., Fielden, L. J. and Degen, A. A. (2005). Energy costs of blood digestion in a host-specific haematophagous parasite. Journal of Experimental Biology 208, 2489–2496.CrossRefGoogle Scholar
Schmidt-Nielsen, K. (1990). Animal Physiology: Adaptation and Environment, 4th Edn. Cambridge University Press, Cambridge, UK.Google Scholar
Smith, C. C. and Fretwell, S. D. (1974). The optimal balance between size and number of offspring. American Naturalist 108, 499–506.CrossRefGoogle Scholar
Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Torres-Vila, L. M. and Rodríguez-Molina, M. C. (2002). Egg size variation and its relationship with larval performance in the Lepidoptera: the case of the European grapevine moth Lobesia botrana. Oikos 99, 272–283.CrossRefGoogle Scholar
Vashchenok, V. S. (1988). Fleas – Vectors of Pathogens Causing Diseases in Humans and Animals. Nauka, Leningrad, USSR (in Russian).Google Scholar
Wiklund, C. and Persson, A. (1983). Fecundity, and the relation of egg weight variation to offspring fitness in the speckled wood butterfly Pararge aegeria, or why don't female butterflies lay more eggs? Oikos 40, 53–63.CrossRefGoogle Scholar
Ziegler, R. and Ibrahim, M. M. (2001). Formation of lipid reserves in fat body and eggs of the yellow fever mosquito, Aedes aegypti. Journal of Insect Physiology 47, 623–627.CrossRefGoogle ScholarPubMed
Ziegler, R. and Van Antwerpen, R. (2006). Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 36, 264–272.CrossRefGoogle ScholarPubMed