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Effects of parasite pressure on parasite mortality and reproductive output in a rodent-flea system: inferring host defense trade-offs

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Abstract

Evaluating host resistance via parasite fitness helps place host-parasite relationships within evolutionary and ecological contexts; however, few studies consider both these processes simultaneously. We investigated how different levels of parasite pressure affect parasite mortality and reproductive success in relationship to host defense efforts, using the rodent Gerbillus nanus and the flea Xenopsylla conformis as a host-parasite system. Fifteen immune-naïve male rodents were infested with 20, 50, or 100 fleas for four weeks. During this time number of new imagoes produced per adult flea (our flea reproductive output metric), flea mortality, and change in circulating anti-flea immunoglobulin G (our measure of adaptive immune defense) were monitored. Three hypotheses guided this work: (1) increasing parasite pressure would heighten host defenses; (2) parasite mortality would increase and parasite reproductive output would decrease with increasing investment in host defense; and (3) hosts under high parasite pressure could invest in behavioral and/or immune responses. We predicted that at high infestation levels (a) parasite mortality would increase; (b) flea reproductive output per individual would decrease; and (c) host circulating anti-flea antibody levels would increase. The hypotheses were partially supported. Flea mortality significantly increased and flea reproductive output significantly decreased as flea pressure increased. Host adaptive immune defense did not significantly change with increasing flea pressure. Therefore, we inferred that investment in host behavioral defense, either alone or in combination with density-dependent effects, may be more efficient at increasing flea mortality and decreasing flea reproductive output than antibody production during initial infestation in this system.

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Acknowledgments

We thank Sergei Burdelov and Asal Kattel for technical assistance as well as the anonymous reviewer for helpful comments. This study was supported by the Israel Science Foundation (grant number 927/13 to AAD, MK, ISK, LK, EG, and RF, and grant number 26/12 to BRK and ISK,). EMW received financial support from the United States-Israel Educational Foundation (USIEF Fulbright Post-Doctoral Fellowship) as well as the Swiss Institute for Dryland Environmental and Energy Research. DK received financial support from the Blaustein Center for Scientific Cooperation. This is publication number 903 of the Mitrani Department of Desert Ecology.

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Authors and Affiliations

  1. 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, 8499000, Midreshet Ben-Gurion, Israel

    Elizabeth M. Warburton, Daniel Kiefer & Boris R. Krasnov

  2. 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, 8499000, Midreshet Ben-Gurion, Israel

    Michael Kam, Irina S. Khokhlova & A. Allan Degen

  3. Department of Animal Sciences, Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem Rehovot, P.O. Box 12, Rehovot, 7610000, Israel

    Enav Bar-Shira & Aharon Friedman

  4. Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, 5290002, Israel

    Lee Koren & Mustafa Asfur

  5. George S. Wise Faculty of Life Sciences, Department of Zoology, Tel Aviv University, Tel Aviv, 6997801, Israel

    Eli Geffen

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  1. Elizabeth M. Warburton
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  2. Michael Kam
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  3. Enav Bar-Shira
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Correspondence to Elizabeth M. Warburton.

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Warburton, E.M., Kam, M., Bar-Shira, E. et al. Effects of parasite pressure on parasite mortality and reproductive output in a rodent-flea system: inferring host defense trade-offs. Parasitol Res 115, 3337–3344 (2016). https://doi.org/10.1007/s00436-016-5093-3

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