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Defining host range: host–parasite compatibility during the non-infective phase of the parasite also matters

  • Jesús Veiga (a1), Paloma De Oña (a1), Beatriz Salazar (a1) and Francisco Valera (a1)

Abstract

Host range and parasite specificity determine key epidemiological, ecological and evolutionary aspects of host–parasite interactions. Parasites are usually classified as generalists or specialists based on the number of hosts they feed on. Yet, the requirements of the various stages of a parasite may influence the suitability of a given host species. Here, we investigate the generalist nature of three common ectoparasites (the dipteran Carnus hemapterus and two species of louse flies, Pseudolynchia canariensis and Ornithophila metallica), exploiting two avian host species (the European roller Coracias garrulus and the Rock pigeon Columba livia), that frequently occupy the same breeding sites. We explore the prevalence and abundance of both the infective and the puparial stages of the ectoparasites in both host species. Strong preferences of Pseudolynchia canariensis for pigeons and of Carnus hemapterus for rollers were found. Moderate prevalence of Ornithophila metallica was found in rollers but this louse fly avoided pigeons. In some cases, the infestation patterns observed for imagoes and puparia were consistent whereas in other cases host preferences inferred from imagoes differed from the ones suggested by puparia. We propose that the adult stages of these ectoparasites are more specialist than reported and that the requirements of non-infective stages can restrict the effective host range of some parasites.

Copyright

Corresponding author

Author for correspondence: Jesús Veiga, E-mail: jveiga@eeza.csic.es

References

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Adang, KL, Oniye, SJ, Ezealor, AU, Abdu, PA, Ajanusi, OJ and Yoriko, KP (2009) Ectoparasites and intestinal helminths of speckled pigeon (Columba guinea) in Zaria, Nigeria. Science World Journal 4, 15.
Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151162.
Amaral, HLC, Bergmann, FB, Silveira, T, dos Santos, PRS and Krüger, RF (2013) Pseudolynchia canariensis (Diptera: Hippoboscidae): distribution pattern and phoretic association with skin mites and chewing lice of Columba livia (Aves: Columbidae). Journal of Natural History 47, 29272936.
Amat-Valero, M, Calero-Torralbo, MA, Václav, R and Valera, F (2014) Cavity types and microclimate: implications for ecological, evolutionary and conservation studies. International Journal of Biometeorology 54, 19831994.
Appelgren, A, McCoy, KD, Richner, H and Doligez, B (2016) Relative fitness of a generalist parasite on two alternative hosts: a cross-infestation experiment to test host specialization of the hen flea Ceratophyllus gallinae (Schrank). Journal of Evolutionary Biology 29, 10911101.
Araujo, SB, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS One 10, e0139225.
Barrett, LG and Heil, M (2012) Unifying concepts and mechanisms in the specificity of plant–enemy interactions. Trends in Plant Science 17, 282292.
Bishopp, FC (1929) The pigeon fly – an important pest of pigeons in the United States. Journal of Economic Entomology 22, 947987.
Boyd, EM (1951) The external parasites of birds: a review. Wilson Bulletin 63, 363369.
Brake, I (2011) World catalog of the family Carnidae (Diptera, Schizophora). Myia 12, 113169.
Brodeur, J, Geervliet, JBF and Vet, LEM (1998) Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomologia Experimentalis et Applicata 86, 145152.
Calero-Torralbo, MA (2011) Factores ecológicos y mecanismos implicados en la variabilidad de la interacción entre un ectoparásito generalista (Carnus hemapterus) y sus hospedadores. PhD thesis. Universidad de Granada.
Calero-Torralbo, MA and Valera, F (2008) Synchronization of host-parasite cycles by means of diapause: host influence and parasite response to involuntary host shifting. Parasitology 135, 13431352.
Calero-Torralbo, MA, Václav, R and Valera, F (2013) Intra-specific variability in life-cycles synchronization between an ectoparasitic fly and its avian host. Oikos 122, 274284.
Cannings, RJ (1986) Infestations of Carnus hemapterus Nitzsch (Diptera: Carnidae) in northern saw-whet owl nests. Murrelet 67, 8384.
Caron, V, Myers, JH and Gillespie, DR (2010) The failure to discriminate: superparasitism of Trichoplusia ni Hübner by a generalist tachinid parasitoid. Bulletin of Entomological Research 100, 255261.
Caswell, H (1983) Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences. American Zoologist 23, 3546.
Coatney, G (1931) On the biology of the pigeon fly, Pseudolynchia maura Bigot (Diptera, Hippoboscidae). Parasitology 23, 525532.
Courtney, SP and Kibota, TT (1990) Mother doesn't know best: selection of plants by ovipositing insects. In Bernays, E (ed). Insect-Plant Interactions. Boca Raton: CRC Press, pp. 161188.
Cramp, S (1998) The Complete Birds of the Western Palearctic on CDROM. Oxford: Oxford University Press.
Dapporto, L and Dennis, RLH (2013) The generalist–specialist continuum: testing predictions for distribution and trends in British butterflies. Biological Conservation 157, 229236.
Dawson, RD and Bortolotti, GR (1997) Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera, Carnidae). Canadian Journal of Zoology 75, 20212026.
Dell Inc. (2016) Dell Statistica (data analysis software system), version 13. Software.dell.com.
Fox, CW and Lalonde, RG (1993) Host confusion and the evolution of insect diet breadths. Oikos 67, 577581.
Grimaldi, D (1997) The bird flies, Genus Carnus: species revision, generic relationships and a fossil Meoneura in amber (Diptera: Carnidae). American Museum Novitates. N° 3190, American Museum of Natural History, New York.
Guiguen, C, Launay, H and Beaucournu, JC (1983) Ectoparasites des oiseaux en Bretagne. I. Répartition et écologie d'un diptère hematophage nouveau pour la France: Carnus hemapterus Nitzsch. Revue Française d'Entomologie 5, 5462.
Harbison, CW and Clayton, DH (2011) Community interactions govern host-switching with implications for host–parasite coevolutionary history. Proceedings of the National Academy of Sciences 108, 95259529.
Harbison, CW, Jacobsen, MV and Clayton, DH (2009) A hitchhiker's guide to parasite transmission: the phoretic behaviour of feather lice. International Journal of Parasitology 39, 569575.
Harwood, RF and James, MT (1979) Entomology in Human and Animal Health, 7th edn. New York, New York, USA: Macmillian, vol. 108, pp. 95259529.
Horner, JD and Abrahamson, WJ (1992) Influence of plant genotype and environment on oviposition preference and offspringsurvival in a gallmaking herbivore. Oecologia 90, 323332.
Hutson, AM (1984) Keds, flat-flies and bat-flies. Diptera, Hippoboscidae and Nycteribiidae. Handbooks for the Identification of British Insects 10, 140.
Johnston, RF and Janiga, M (1995) Feral Pigeons. New York, USA: Oxford University Press, 320pp.
Jorge, LR, Prado, PI, Almeida-Neto, M and Lewinsohn, TM (2014) An integrated framework to improve the concept of resource specialisation. Ecology Letters 17, 13411350.
Kaunisto, S, Raunismaa, I, Kortet, R and Ylönen, H (2016) Summer time predation on the obligatory off-host stage of an invasive ectoparasite. Parasitology 143, 19601973.
Kirkpatrick, CE and Colvin, BA (1989) Ectoparasitic fly Carnus hempaterus (Diptera: Carnidae) in a nesting population of common barn owls (Strigiformes: Tytonidae). Journal of Medical Entomology 26, 109112.
Klei, TR and Degiusti, DL (1975) Observations on the bionomics of Pseudolynchia canariensis (Diptera: Hippoboscidae). Parasitology 70, 195202.
Kortet, R, Härkönen, L, Hokkanen, P, Härkönen, S, Kaitala, A, Kaunisto, S, Laaksonen, S, Kekäläinen, J and Ylönen, H (2010) Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bulletin of Entomological Research 100, 279285.
Krasnov, BR, Khokhlova, IS, Burdelova, NV, Mirzoyan, NS and Degen, AA (2004) Fitness consequences of host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. Journal of Animal Ecology 73, 815820.
Lázaro, R, Rodrigo, FS, Gutiérrez, L, Domingo, F and Puigdefábregas, J (2001) Analysis of a thirty-year rainfall record (1967–1997) from semi-arid SE Spain: a plant ecological perspective. Journal of Arid Environments 48, 373395.
Lázaro, R, Rodríguez-Tamayo, ML, Ordiales, R, Puigdefábregas, J (2004) El clima. In Mota, J, Cabello, J, Cerrillo, MI and Rodríguez-Tamayo, ML (eds), Subdesiertos de Almería: naturaleza de cine. Junta de Andalucía, Spain: Consejería de Medio Ambiente, pp. 6379.
Lehane, MJ (2005) The Biology of Blood-sucking in Insects, 2nd edn. New York, USA: Cambridge University Press, 336 pp.
Lemoine, M, Doligez, B, Passerault, M and Richner, H (2011) Influence of host profitability and microenvironmental conditions on parasite specialization on a main and an alternative hosts. Journal of Evolutionary Biology 24, 12121225.
Liker, A, Markus, M, Vozár, A, Zemankovics, E and Rózsa, L (2001) Distribution of Carnus hemapterus in a starling colony. Canadian Journal of Zoology 79, 574580.
Lloyd, J (2002) Louse flies, keds, and related flies (Hippoboscoidea). In Mullen, G and Durden, L (eds), Medical and Veterinary Entomology. Boston, USA: Academic Press, pp. 349362.
Loxdale, D and Harvey, JA (2016) The “generalism” debate: misinterpreting the term in the empirical literature focusing on dietary breadth in insects. Biological Journal of the Linnean Society 119, 265282.
Maa, TC (1966) On the Genus Pseudolynchia bequaert (Diptera: Hippoboscidae). Pacific Insects Monograph 10, 125138.
Maa, TC (1969) Synopses of the genera Ornithophila and Ornithoctona with remarks on their habitat diversification (Diptera: Hippoboscidae). Pacific Insects Monograph 20, 123.
Mandal, FB (1989) Prepupae and pupal development of Pseudolynchia canariensis (Macquart) (Diptera: Hippoboscidae). Environment and Ecology 7, 733735.
McCoy, KD, Léger, E and Dietrich, M (2013) Host specialization in ticks and transmission of tick-borne diseases: a review. Frontiers in Cellular and Infection Microbiology 3, 57.
O'Connor, LJ, Walkden-Brown, SW and Kahn, LP (2006) Ecology of the free-living stages of major trichostrongylid parasites of sheep. Veterinary Parasitology 142, 115.
Papp, L (1998) Family Carnidae. In Papp, L and Darvas, B (eds), Manual of Palaearctic Diptera. Budapest: Science Herald, vol. 3, pp. 211217.
Pietrock, M and Marcogliese, DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.
Reiczigel, J and Rózsa, L (2005) Quantitative Parasitology 3.0. Budapest: Distributed by the authors.
Roulin, A (1998) Cycle de reproduction et abondance du diptère parasite Carnus hemapterus dans les nicheés de chouettes effraies Tyto alba. Alauda 66, 265272.
Soler, JJ, Møller, AP, Soler, M and Martínez, JG (1999) Interactions between a brood parasite and its host in relation to parasitism and immune defence. Evolutionary Ecology Research 1, 189210.
Soltész, Z, Seres, N and Kovács-Hostyánszki, A (2018) Dipteran assemblages in Red-Footed Falcon (Falco vespertinus) nest boxes. Acta Zoologica Adademiae Scientiarum Hungaricae 64, 91102.
Sosnowski, J and Chmielewski, S (1996) Breeding biology of the Roller (Coracias garrulus) in the Puscza Pilicka forest, central Poland. Acta Ornithologica 31, 119131.
Thompson, JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring inphytophagous insects. Entomologia Experimentalis et Applicata 47, 314.
Václav, R, Calero-Torralbo, MA and Valera, F (2008) Ectoparasite load is linked to ontogeny and cell-mediated immunity in an avian host system with pronounced hatching asynchrony. Biological Journal of the Linnean Society 94, 463473.
Václav, R, Valera, F and Martínez, T (2011) Social information in nest colonisation and occupancy in a long-lived, solitary breeding bird. Oecologia 165, 617627.
Valera, F, Casas-Crivillé, A and Hoi, H (2003) Interspecific parasite exchange in a mixed colony of birds. Journal of Parasitology 89, 245250.
Valera, F, Casas-Crivillé, A and Calero-Torralbo, MA (2006) Prolonged diapause in the ectoparasite Carnus hemapterus: how frequent is it in parasites? Parasitology 133, 179188.
Valera, F, Veiga, J, Sandoval, A and Moreno, E (2018) Coexistence, habitat associations and puparia description of three dipteran species of the Family Carnidae. Parasitology Open 4, e1, 1–9.
Veiga, J, Moreno, E, Benzal, J and Valera, F (2018) Off-host longevity of the winged dispersal stage of Carnus hemapterus (Insecta: Diptera) modulated by gender, body size and food provisioning. Parasitology. doi: 10.1017/S0031182018001300.
Waite, JL, Henry, AR and Clayton, DH (2012) How effective is preening against mobile ectoparasites? An experimental test with pigeons and hippoboscid flies. International Journal for Parasitology 42, 463467.
Ward, SA, Leather, SR, Pickup, J and Harrington, R (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology 67, 763773.
Whitworth, TL (1976) Host and habitat preferences, life history, pathogenicity and population regulation in species of Protocallyphora Hough (Diptera: Calliphoridae) (PhD thesis). Utah State University, Logan, 157 pp.
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