Abstract
To understand whether a parasite can exploit a novel invasive host species, we measured reproductive performance (number of eggs per female per day, egg size, development rate and size of new imagoes) of fleas from the Negev desert in Israel (two host generalists, Synosternus cleopatrae and Xenopsylla ramesis, and a host specialist, Parapulex chephrenis) when they exploited either a local murid host (Gerbillus andersoni, Meriones crassus and Acomys cahirinus) or two alien hosts (North American heteromyids, Chaetodipus penicillatus and Dipodomys merriami). We asked whether (1) reproductive performance of a flea differs between an alien and a characteristic hosts and (2) this difference is greater in a host specialist than in host generalists. The three fleas performed poorly on alien hosts as compared to local hosts, but the pattern of performance differed both among fleas and within fleas between alien hosts. The response to alien hosts did not depend on the degree of host specificity of a flea. We conclude that successful parasite colonisation of an invasive host is determined by some physiological, immunological and/or behavioural compatibility between a host and a parasite. This compatibility is unique for each host-parasite association, so that the success of a parasite to colonise an invasive host is unpredictable.
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References
Berrigan D (1991) The allometry of egg size and number in insects. Oikos 60:31–21. https://doi.org/10.2307/3545073
Boycott AE (1913) The reaction of flea bites. J Pathol Bacteriol 17:110
Brooks DR, León-Règagnon V, McLennan DA, Zelmer D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87:S76–S85. https://doi.org/10.1890/0012-9658(2006)87[76:EFAADO]2.0.CO;2
Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago
Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39. https://doi.org/10.1111/j.1523-1739.1988.tb00333.x
Dryden MW (1989) Host association, on-host longevity and egg production of Ctenocephalides felis felis. Vet Parasitol 34:117–122. https://doi.org/10.1016/0304-4017(89)90171-4
Dunsmore J (1981) The role of parasites in population regulation of the European rabbit (Oryctolagus cuniculus) in Australia. In: Chapman JA, Pursley D (eds) Worldwide Furbearers Conference Proceedings held in Frostburg, Maryland, August 1980, 654–69
Feingold BF, Benjamini E, Michaeli D (1968) The allergic responses to insect bites. Annu Rev Entomol 13:138–158
Genoways HH, Brown JH (1993) Biology of the heteromyidae. The American Society of Mammologists, Lawrence KS. Special Publication No. 10
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proc R Soc Lond B Biol Sci 268:2071–2075. https://doi.org/10.1098/rspb.2001.1686
Giron D, Casas J (2003) Mothers reduce egg provisioning with age. Ecol Lett 6:273–277
Grigulis K, Sheppard AW, Ash JE, Groves RH (2001) The comparative demography of the pasture weed Echium plantagineum between its native and invaded ranges. J Appl Ecol 38:281–290. https://doi.org/10.1046/j.1365-2664.2001.00587.x
Gruner DS (2005) Biotic resistance to an invasive spider conferred by generalist insectivorous birds on Hawai’i Island. Biol Invasions 7:541–546. https://doi.org/10.1007/s10530-004-2509-2
Harrington LC, Edman JD, Scott TW (2001) Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 38:411–422. https://doi.org/10.1603/0022-2585-38.3.411
Hart BL, Hart LA, Mooring MS, Olubayo R (1992) Biological basis of grooming behaviour in antelope: the body-size, vigilance and habitat principles. Anim Behav 44:615–631
Herrera AM, Carruthers RI, Mills NJ (2011) Introduced populations of Genista monspessulana (French broom) are more dense and produce a greater seed rain in California, USA, than native populations in the Mediterranean Basin of Europe. Biol Invasions 13:369–380. https://doi.org/10.1007/s10530-010-9829-1
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Hsu M-H, Hsu T-C, Wu W-J (2002) Distribution of cat fleas (Siphonaptera: Pulicidae) on the cat. J Med Entomol 39:685–688
Hudson BW, Feingold BF, Kartman L (1960a) Allergy to flea bites. I. Experimental induction of flea-bite sensitivity in guinea pigs. Exp Parasitol 9:18–24
Hudson BW, Feingold BF, Kartman L (1960b) Allergy to flea bites: II. Investigations of flea bite sensitivity in humans. Exp Parasitol 9:264–270
Jakobs GE, Weber E, Edwards PJ (2004) Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Divers Distrib 10:11–19. https://doi.org/10.1111/j.1472-4642.2004.00052.x
Jernelöv A (2017) Rabbits in Australia. In: Jernelöv A (ed) The long-term fate of invasive species. Springer, Cham, pp 73–89
Jones CJ (1996) Immune responses to fleas, bugs and sucking lice. In: Wikel SK (ed) The immunology of host-ectoparasitic arthropod relationships. CAB International, Wallingford, pp 150–174
Khokhlova IS, Spinu M, Krasnov BR, Degen AA (2004a) Immune response to fleas in a wild desert rodent: effect of parasite species, parasite burden, sex of host and host parasitological experience. J Exp Biol 207:2725–2733
Khokhlova IS, Spinu M, Krasnov BR, Degen AA (2004b) Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitol Res 94:304–311
Khokhlova IS, Ghazaryan L, Krasnov BR, Degen AA (2008) Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent infesting fleas. Funct Ecol 22:530–536. https://doi.org/10.1111/j.1365-2435.2008.01393.x
Khokhlova IS, Serobyan V, Krasnov BR, Degen AA (2009a) Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitol Res 105:1667–1673. https://doi.org/10.1007/s00436-009-1608-5
Khokhlova IS, Serobyan V, Krasnov BR, Degen AA (2009b) Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus? J Exp Biol 212:1429–1435. https://doi.org/10.1242/jeb.029389
Khokhlova IS, Serobyan V, Degen AA, Krasnov BR (2010a) Host gender and offspring quality in a flea parasitic on a rodent. J Exp Biol 213:3299–3304. https://doi.org/10.1242/jeb.046565
Khokhlova IS, Ghazaryan L, Degen AA, Krasnov BR (2010b) Infestation experience of a rodent host and offspring viability of fleas: variation among host–parasite associations. J Exp Zool A Ecol Genet Physiol 313:680–689. https://doi.org/10.1002/jez.640
Khokhlova IS, Fielden LJ, Degen AA, Krasnov BR (2012) Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. J Evol Biol 25:2005–2013. https://doi.org/10.1111/j.1420-9101.2012.02577.x
Krasnov BR, Shenbrot GI, Medvedev SG, Vatschenok VS, Khokhlova IS (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. https://doi.org/10.1017/S0031182096008347
Krasnov BR, Hastriter M, Medvedev SG, Shenbrot GI, Khokhlova IS, Vatshchenok VS (1999) Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel J Zool 45:333–340
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Med Vet Entomol 15:249–258. https://doi.org/10.1046/j.0269-283x.2001.00295.x
Krasnov BR, Khokhlova IS, Oguzoglu I, Burdelova NV (2002) Host discrimination by two desert fleas using an odour cue. Anim Behav 64:33–40. https://doi.org/10.1006/anbe.2002.3030
Krasnov BR, Sarfati M, Arakelyan MS, Khokhlova IS, Burdelova NV, Degen AA (2003a) Host-specificity and foraging efficiency in blood-sucking parasite: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitol Res 90:393–399. https://doi.org/10.1007/s00436-003-0873-y
Krasnov BR, Khokhlova IS, Shenbrot GI (2003b) Density-dependent host selection in ectoparasites: an application of isodar theory to fleas parasitizing rodents. Oecologia 134:365–373. https://doi.org/10.1007/s00442-002-1122-2
Krasnov BR, Shenbrot GI, Khokhlova IS, Poulin R (2004) Relationships between parasite abundance and the taxonomic distance among a parasite’s host species: an example with fleas parasitic on small mammals. Int J Parasitol 34:1289–1297. https://doi.org/10.1016/j.ijpara.2004.08.003
Krasnov BR, Korine C, Burdelova NV, Khokhlova IS, Pinshow B (2007) Between-host phylogenetic distance and feeding efficiency in hematophagous ectoparasites: rodent fleas and a bat host. Parasitol Res 101:365–371. https://doi.org/10.1007/s00436-007-0480-4
Lehane MJ (2005) The biology of blood-sucking in insects, 2nd edn. Cambridge University Press, Cambridge
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
Mans BJ, Louw AI, Neitz AWH (2002) Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Mol Biol Evol 19:1695–1705
Nuismer SL, Thompson JN (2006) Coevolutionary alternation in antagonistic interactions. Evolution 60:2207–2217. https://doi.org/10.1554/06-111.1
Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alter native acanthocephalan infections in native fish. J Anim Ecol 80:990–998. https://doi.org/10.1111/j.1365-2656.2011.01834.x
Paterson RA, Lal A, Dale M, Townsend CR, Poulin R, Tompkins DM (2013) Relative competence of native and exotic fish hosts for two generalist native trematodes. Int J Parasitol Parasites Wildl 2:136–143. https://doi.org/10.1016/j.ijppaw.2013.03.004
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0, URL http://www.R-project.org/
Ribeiro JMC (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 4:143–152
Ribeiro JMC, Vaughan JA, Farhang-Azad A (1990) Characterization of the salivary apyrase activity of three rodent flea species. Comp Biochem Physiol B 95:215–218
Soler JJ, Aviles JM, Soler M, Møller AP (2003) Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo. Biol J Linn Soc 79:551–563
Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37. https://doi.org/10.1111/j.1365-2745.2004.00962.x
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128. https://doi.org/10.1079/JOH2006364
Thébaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236. https://doi.org/10.1086/318635
Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago
Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345. https://doi.org/10.1023/A:1015855019360
van der Mescht L, Khokhlova IS, Warburton EW, Krasnov BR (2017) Parasite performance and host alternation: is there a negative effect in host-specific and host-opportunistic parasites? Parasitology 144:1107–1116. https://doi.org/10.1017/S0031182017000373
Vashchenok VS (2001) Age changes of fecundity in fleas Leptopsylla segnis (Siphonaptera: Leptopsyllidae). Parazitologiya 35:460–464 (in Russian)
Vashchenok VS, Solina LT, Zhirnov AE (1976) Digestion of blood of different animals by fleas Xenopsylla cheopis. Parazitologiya 10:544–549 (in Russian)
Webber LA, Edman JD (1972) Anti-mosquito behaviour of ciconiiform birds. Anim Behav 20:228–232
Zolotova SI, Bibikova VI, Murzakhmetova K (1979) On the fecundity of fleas Xenopsylla gerbilli minax (Aphaniptera), parasites of the great gerbil. Parazitologiya 13:497–502
Funding
This study was supported by the Israel Science Foundation (grant number 149/17 to BRK and ISK). LVDM received financial support from the Blaustein Center for Scientific Cooperation and the French Associates Institute for Agriculture and Biotechnology of Drylands. EMW received financial support from the Blaustein Center for Scientific Cooperation. This is publication no. 966 of the Mitrani Department of Desert Ecology.
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All experimental procedures met the requirements of the 1994 Law for the Prevention of Cruelty to Animals (Experiments on Animals) of the State of Israel and were approved by the Ben-Gurion University Committee for the Ethical Care and Use of Animals in Experiments under permit IL-11-02-14 issued to BPK and ISK.
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van der Mescht, L., Khokhlova, I.S., Warburton, E.M. et al. Can we predict the success of a parasite to colonise an invasive host?. Parasitol Res 117, 2305–2314 (2018). https://doi.org/10.1007/s00436-018-5921-8
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DOI: https://doi.org/10.1007/s00436-018-5921-8