Skip to main content Accessibility help
×
×
Home

Off-host longevity of the winged dispersal stage of Carnus hemapterus (Insecta: Diptera) modulated by gender, body size and food provisioning

  • Jesús Veiga (a1), Eulalia Moreno (a1), Jesús Benzal (a1) and Francisco Valera (a1)

Abstract

Highlighting the dispersal ecology of parasites is important for understanding epidemiological, demographic and coevolutionary aspects of host–parasite interactions. Yet, critical aspects of the dispersal stage of parasites, such as longevity and the factors influencing it, are poorly known. Here we study the lifespan of the dispersal stage of an ectoparasitic dipteran, Carnus hemapterus, and the impact of gender, body size and food provisioning on longevity. We found that freshly emerged imagoes survive at most less than 4 days. Longevity increased with body size and, since this parasite exhibits sexual size dimorphism, the bigger females lived longer than males. However, controlling for body size suggests that males lived relatively longer than females. Furthermore, a humid environment and food provisioning (flowers) significantly increased individual life spans. We discuss the relative importance of spatial and temporal dispersal in relation to the infectious potential of this parasite.

Copyright

Corresponding author

Author for correspondence: Francisco Valera, E-mail: pvalera@eeza.csic.es

References

Hide All
Blanckenhorn, WU, Preziosi, RF and Fairbairn, DJ (1995) Time and energy constraints and the evolution of sexual size dimorphism – to eat or to mate? Evolutionary Ecology 9, 369381.
Bohonak, AJ and Jenkins, DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters 6, 783796.
Botzler, RG and Brown, RN (2014) Foundations of Wildlife Diseases. Oakland, California, USA: University of California Press.
Brake, I (2011) World catalog of the family Carnidae (Diptera, Schizophora). Myia 12, 113169.
Briegel, H and Horler, E (1993) Multiple blood meals as reproductive strategy in Anopheles (Diptera, Culicidae). Journal of Medical Entomology 30, 975985.
Brown, CR and Brown, MB (1996) Coloniality in the Cliff Swallow: The Effect of Group Size on Social Behaviour. Chicago, Illinois, USA: University of Chicago Press.
Brown, CR and Brown, MB (2004) Group size and ectoparasitism affect daily survival probability in a colonial bird. Behavioral Ecology and Sociobiology 56, 498511.
Bujan, J, Yanoviak, SP and Kaspari, M (2016) Dessication resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community. Ecology and Evolution 6, 62826291.
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, Granada, Spain.
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.
Carroll, AL and Quiring, DT (1993) Interactions between size and temperature influence fecundity and longevity of a tortricid moth, Zeiraphera canadensis. Oecologia 93, 233241.
Chen, L, Onagbola, EO and Fadamiro, HY (2005) Effects of temperature, sugar availability, gender, mating, and size on the longevity of phorid fly Pseudacteon tricuspis (Diptera: Phoridae). Environmental Entomology 34, 246255.
Clayton, DH, Lee, PLM, Tompkins, DM and Brodie, ED III (1999) Reciprocal natural selection on host-parasite phenotypes. The American Naturalist 154, 261270.
Clements, AN (1955) The sources of energy for flight in mosquitoes. Journal of Experimental Biology 32, 547554.
Compton, SG (2002) Sailing with the wind: dispersal by small flying insects. In Bullock, D (ed.) Dispersal Ecology. Oxford, UK: British Ecological Society, Blackwells, pp. 113133.
Cônsoli, FL and Parra, JRP (1995) Effects of constant and alternating temperatures on Trichogramma galloi Zucchi (Hym., Trichogrammatidae) biology. II. Parasitism capacity and longevity. Journal of Applied Entomology 119, 667670.
Darwin, C (1871) The Descent of Man, and Selection in Relation to Sex. London: John Murray.
Dell Inc (2016) Dell Statistica (data analysis software system), version 13. Software.dell.com.
Dudley, R (2000) The Biomechanics of Insect Flight. Princeton, New Jersey, USA: Princeton University Press.
Fairbairn, DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659687.
Foster, WA (1995) Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology 40, 443474.
Fox, CW, Dublin, L and Pollitt, SJ (2003) Gender differences in lifespan and mortality rates in two seed beetle species. Functional Ecology 17, 619626.
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, pp. 30. 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.
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349364.
Hairston, NG (2000) Temporal dispersal: ecological and evolutionary implications of prolonged egg diapause. American Zoologist 40, 10391040.
Hairston, NG and Kearns, CM (2002) Temporal dispersal: ecological and evolutionary aspects of zooplankton egg banks and the role of sediment mixing. Integrative and Comparative Biology 42, 481491.
Hanski, I (1988) Four kinds of extra long diapause in insects: a review of theory and observations. Annales Zoologici Fennici 25, 3753.
Harper, GH, Marchant, A and Boddington, DG (1992) The ecology of the hen flea Ceratophyllus gallinae and the moorhen flea Dasypsyllus gallinulae in nest boxes. Journal of Animal Ecology 61, 317327.
Hassell, MP (2000) The Spatial and Temporal Dynamics of Host-Parasitoid Interactions. Oxford, UK: Oxford University Press.
Hasson, E, Fanara, JJ, Rodriguez, C, Vilardi, JC, Reig, OA and Fontdevila, A (1993) The evolutionary history of Drosophila buzzatii. XXVII. Thorax length is positively correlated with longevity in a natural population from Argentina. Genetics 92, 6165.
Hoi, H, Kristofík, J, Darolová, A and Hoi, C (2010) Are parasite intensity and related costs of the milichiid fly Carnus hemapterus related to host sociality? Journal of Ornithology 151, 907913.
Johnson, CG (1969) Migration and Dispersal of Insects by Flight. London, UK: Methuen.
Kirkpatrick, CE and Colvin, BA (1989) Ectoparasitic fly Carnus hemapterus (Diptera: Carnidae) in a nesting population of common barn-owls (Strigiformes: Tytonidae). Journal of Medical Entomology 26, 109112.
Kjellberg, F, Doumesche, B and Bronstein, JL (1988) Longevity of a fig wasp (Blastophaga psenes). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen C91, 117122.
Kleindorfer, S and Dudaniec, RY (2009) Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin's tree finches. Behavioral Ecology and Sociobiology 63, 731739.
Lessard, E and Boivin, G (2013) Effect of low temperature on emergence, fecundity, longevity and host-feeding by Trichogramma brassicae. BioControl 58, 319329.
Lessells, CM and Boag, PT (1987) Unrepeatable repeatabilities: a common mistake. The Auk 104, 116121.
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.
Manda, H, Gouagna, LC, Foster, WA, Jackson, RR, Beier, JC, Githure, JI and Hassanali, A (2007) Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malaria Journal 6, 113.
McCoy, KD, Boulinier, T, Tirard, C and Michalakis, Y (2003) Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288296.
Mellanby, K (1932) The influence of atmospheric humidity on the thermal death point of a number of insects. Journal of Experimental Biology 9, 222231.
Nilssen, AC (1997) Factors affecting size, longevity and fecundity in the reindeer oestrid flies Hypoderma tarandi (L.) and Cephenemyia trompe (Modeer). Ecological Entomology 22, 294304.
Papp, L (1998) Family carnidae. In Papp, L and Darvas, B (eds), Manual of Palaearctic Diptera. Budapest: Science Herald, vol. 3, pp. 211217.
Roff, D (1993) The Evolution of Life Histories. Theory and Analysis. New York, USA: Springer.
Roulin, A (1998) Cycle de reproduction et abondance du diptère parasite Carnus hemapterus dans les nicheés de chouettes effraies Tyto alba. Alauda 66, 265272.
Roulin, A (1999) Fécondité de la mouche Carnus hemapterus, ectoparasite des jeunes chouettes effraies Tyto alba. Alauda 67, 205212.
Sivinski, JM (1993) Longevity and fecundity in the Caribbean fruit fly (Diptera: Tephritidae): effects of mating, strain and body size. Florida Entomologist 76, 635644.
Soltész, Z, Seres, N and Kovács-Hostyánszki, A (2018) Dipteran assemblages in Red-footed Falcon (Falco vespertinus) nest boxes. Acta Zoologica Academiae Scientiarum Hungaricae 64, 91102.
Taylor, F (1981) Ecology and evolution of physiological time in insects. American Naturalist 117, 123.
Tochen, S, Woltz, JM, Dalton, DT, Lee, JC, Wiman, NG and Walton, VM (2015) Humidity affects population of Drosophyla suzukii (Diptera: Drosophylae) in blueberry. Journal of Applied Entomology 140, 4757.
Tochen, S, Walton, VM and Lee, JC (2016) Impact of floral feeding on adult Drosophila suzukii survival and nutrient status. Journal of Pest Science 89, 793802.
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.
Valera, F and Zídková, L (2012) Reproductive anatomy and fecundity estimation of the haematophagous ectoparasite Carnus hemapterus. Parasitology Research 110, 17331739.
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.
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.
Winkler, K, Wäckers, F, Bukovinszkine-Kissa, G and van Lenteren, J (2006) Sugar resources are vital for Diadegma semiclausum fecundity under field conditions. Basic and Applied Ecology 7, 133140.
Wright, GA and Schiestl, FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology 23, 841851.
Yu, BT, Ding, YM, Mo, XC, Liu, N, Li, HJ and Mo, JC (2016) Survivorship and fecundity of Culex pipiens pallens feeding on flowering plants and seed pods with differential preferences. Acta Tropica 155, 5157.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed